Manganese Compounds as Water-Oxidizing ... - ACS Publications

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Manganese Compounds as Water-Oxidizing Catalysts: From the Natural Water-Oxidizing Complex to Nanosized Manganese Oxide Structures Mohammad Mahdi Najafpour,*,†,‡ Gernot Renger,§ Małgorzata Hołyńska,∥ Atefeh Nemati Moghaddam,† Eva-Mari Aro,⊥ Robert Carpentier,# Hiroshi Nishihara,○ Julian J. Eaton-Rye,∇ Jian-Ren Shen,□,▲ and Suleyman I. Allakhverdiev*,●,■,◇ †

Department of Chemistry, and ‡Centre of Climate Change and Global Warming, Institute for Advanced Studies in Basic Sciences (IASBS), Zanjan 45195-1159, Iran § Institute of Chemistry, Max-Volmer-Laboratory of Biophysical Chemistry, Technical University Berlin, Straße des 17. Juni 135, D-10623 Berlin, Germany ∥ Fachbereich Chemie und Wissenschaftliches Zentrum für Materialwissenschaften (WZMW), Philipps-Universität Marburg, Hans-Meerwein-Straße, D-35032 Marburg, Germany ⊥ Department of Biochemistry and Food Chemistry, University of Turku, 20014 Turku, Finland # Groupe de Recherche en Biologie Végétale (GRBV), Université du Québec à Trois-Rivières, C.P. 500, Trois-Rivières, Québec G9A 5H7, Canada ○ Department of Chemistry, School of Science, The University of Tokyo, 7-3-1, Hongo, Bunkyo-Ku, Tokyo 113-0033, Japan ∇ Department of Biochemistry, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand □ Photosynthesis Research Center, Graduate School of Natural Science and Technology, Faculty of Science, Okayama University, Okayama 700-8530, Japan ▲ Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China ● Controlled Photobiosynthesis Laboratory, Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia ■ Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region 142290, Russia ◇ Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow 119991, Russia ABSTRACT: All cyanobacteria, algae, and plants use a similar water-oxidizing catalyst for water oxidation. This catalyst is housed in Photosystem II, a membrane-protein complex that functions as a light-driven water oxidase in oxygenic photosynthesis. Water oxidation is also an important reaction in artificial photosynthesis because it has the potential to provide cheap electrons from water for hydrogen production or for the reduction of carbon dioxide on an industrial scale. The water-oxidizing complex of Photosystem II is a Mn−Ca cluster that oxidizes water with a low overpotential and high turnover frequency number of up to 25−90 molecules of O2 released per second. In this Review, we discuss the atomic structure of the Mn−Ca cluster of the Photosystem II water-oxidizing complex from the viewpoint that the underlying mechanism can be informative when designing artificial water-oxidizing catalysts. This is followed by consideration of functional Mn-based model complexes for water oxidation and the issue of Mn complexes decomposing to Mn oxide. We then provide a detailed assessment of the chemistry of Mn oxides by considering how their bulk and nanoscale properties contribute to their effectiveness as water-oxidizing catalysts.

CONTENTS 1. 2. 3. 4. 5.

Introduction Reaction Mechanism of Water Oxidation in PSII Energetics of Water Oxidation Cofactor Arrangement in PSII Oxidation of YZ by P680+ © 2016 American Chemical Society

6. Assembly, Structure, and Function of the WOC 6.1. Assembly and Decomposition of the WOC 6.2. Structure and Function of the WOC

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Received: June 13, 2015 Published: January 26, 2016 2886

DOI: 10.1021/acs.chemrev.5b00340 Chem. Rev. 2016, 116, 2886−2936

Chemical Reviews 6.2.1. Structure of the Catalytic Mn 4 CaO x Cluster 6.2.2. Coordination Sphere of the Mn4CaOx Cluster 6.2.3. Electronic Structure and Nuclear Arrangement for the Si States of the Catalytic Site 6.2.4. Kinetic Aspects of the Water-Oxidation Process 6.2.5. Substrate/Product Pathways 6.2.6. Mechanistic Aspects of the Water-Oxidation Process 7. Lessons Learned from the WOC To Assist Artificial Water Oxidation 7.1. Mnn+ and Ca2+: Abundant and Environmentally Friendly Ions 7.2. A Heterogeneous or a Homogeneous Catalyst 7.3. Tetranuclear Mn Structure for the WOC in PSII 7.4. The pH Issue in the Water-Oxidation Reaction 7.5. Proton-Coupled Electron Transfer in Biological Water Oxidation 7.6. Channels in PSII 7.7. Spin-Flipping Theory in Chemical Reactions 7.8. The Nanoscale of the Mn−Ca Cluster 7.9. Oxidant 7.10. Outer Bonds in the Biological Water Oxidation by PSII 7.11. Roles of Ca2+ and Cl− in PSII 7.12. A Four-Electron Water-Oxidation Mechanism 7.13. Redox Accumulation in the WOC 7.14. Regulating the Oxidizing Power in Each Charge-Accumulation Step 7.15. Amino Acid Side Chains 7.16. Binding Sites for Water Molecules 7.17. Photosystem II as a Photoassembled Complex 7.18. Chemistry of Mn 7.19. Self-Repair 7.20. A Different Strategy To Protect from Light 7.21. Vibrations in Enzyme-Catalyzed Reactions 8. Artificial Models 8.1. Oxidants in Water Oxidation 8.1.1. Ru(bpy)33+ 8.1.2. Cerium(IV) Ammonium Nitrate (CAN) 8.1.3. Other Oxidants 8.2. Models 8.2.1. Mn−Schiff Base Complexes 8.2.2. [(OH2)(terpy)Mn(μ-O)2Mn(terpy)(OH2)]3+ 8.2.3. A Mn−Oxo Cube from the Laboratory of Dismukes 8.2.4. Mn−Porphyrin Complexes as WaterOxidizing Catalysts 8.2.5. A Structural and Functional Dinuclear Model for the WOC 8.2.6. Nanosized Mn Oxide: A Proposed True Catalyst for Water Oxidation 8.2.7. Mn Oxides 9. Immobilization of PSII on the Surface of Electrodes 10. Non-Biomimetic Water-Oxidizing Catalysts 11. Brief Concluding Remark Author Information

Review

Corresponding Authors Notes Biographies Acknowledgments Dedication Abbreviations References

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1. INTRODUCTION Increasing consumption of fossil fuels not only causes significant environmental problems, but it is also expected to cause the ultimate depletion of fossil fuels within 50−150 years.1 Energy security is, accordingly, a high priority for world economies, and it is evident that new sources of energy will be needed in the near future. Wind, ocean currents, tides, and waves are all potential sources of energy, but by far the largest energy source available on Earth is the light energy from the sun. In fact, a fraction of a percentage of the total solar energy that the Earth receives will be enough to fulfill our energy consumption.2 Consequently, the development of an efficient conversion and storage strategy that will enable the use of intermittent and fluctuating energy supplies is urgently required. An intriguing potential solution to the expected shortfall in energy supplies is artificial photosynthesis,3 whereby light energy can be stored in chemical bonds and, hence, be made available as fuels.4−8 One of the most important goals of artificial photosynthesis is to use water as the electron and hydrogen donor, just as is done in natural photosynthesis. Generally, water splitting is performed in three different ways: chemically, electrochemically, and photochemically. Of various proposed systems, photochemical water splitting is the only one that can use solar energy and then store this in the form of H2 (see eqs 1−3):9−11

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The key point in both natural and artificial photosynthesis is the utilization of water as a cheap and ultimate source of electrons.12−15 In this Review, we will consider the thermodynamically challenging reaction of water oxidation by natural and artificial Mn-based catalysts.16−18 To illustrate the peculiarities of oxidative water splitting in natural photosynthesis, it is useful to compare the reaction mechanism with that of the general reaction pathway of this process via a sequence of four one-electron redox steps in aqueous solution. Figure 1 schematically illustrates this process. This scheme leads to the following conclusions: (i) a proton transfer accompanies each step of the redox processes so that the energetics of all reaction steps are pH-dependent; and (ii) the four-step sequence generates various reactive oxygen species (ROS) as intermediates, HO•, H2O2, and HO2/O2•−. These ROS are highly reactive and harmful to biological materials (e.g., nucleic acids, proteins, and lipids); for this reason, their accumulation in living organisms must be minimized. The energy diagram for these processes is shown in Figure 1A (top, right-hand side). Considerable differences in the Gibbs free energy (ΔG°) parameters of the reaction steps are observed.19 The removal of the first electron from an H2O molecule has a midpoint potential of +2.3 V at pH 7.0 and is accompanied by loss of a proton, producing an HO• radical. Hence, the energy of photons corresponding to red light (e.g., a photon at a

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P680 is not simple,32 and different individual pathways may be used to form the ion-radical pair P680+Pheo−.32−36 The oxidizing equivalents generated at the donor side of PSII (denoted by ⊕) are used to split water, as shown in eq 6, while the reducing equivalents accumulated (denoted by Θ) at the acceptor side of PSII are used to reduce plastoquinone to plastoquinol (eq 7). H+Lumen and H+Stroma stand for the transfer of protons from the cytosol/stroma (the outer part of the thylakoids) into the lumen (the inner part of the thylakoids). A breakthrough in the research on the mechanism of water oxidation was the discovery that excitation of dark-adapted algal cells or plant chloroplasts with a series of single-turnover flashes produced oxygen with a characteristic period-four oscillation pattern, in which the maximum O2 yield was obtained after the third, seventh, 11th, etc., flashes (Figure 1B).37 In 1970, Kok and co-workers38 interpreted this feature using a model in which the oxidative water splitting in PSII takes place via a four-step reaction sequence comprising five intermediate states (from S0 to S4). In this scheme, which is referred to as the Kok cycle or the Sstate cycle, S0 reflects the most reduced state and S4 the most oxidized state; states S1, S2, and S3 correspond to intermediary redox levels during water oxidation in solution. The oscillation pattern was damped because of mishits (represented by the miss factor α) and double hits (β) in the transition from the Si to the Si+1 state. Likewise, the maximum oxygen yield after the third flash revealed that, in the dark, the WOC relaxes to the redox state S1 rather than to S0.39−42 In these earlier studies, it was proven that every P680+ corresponds to only one WOC through experiments showing that the pattern of flash-induced oxygen yield does not change as a function of the content of competent PSII complexes. In addition, the coupling between P680+ and the WOC has been shown to be mediated by the redox-active tyrosine YZ.43,44 The mishits in the Si-state transitions originate from the transiently blocked RCs (“closed RCs”) during the actinic flash because of the existence of a population of P680+ and/or QA− via dynamic equilibria at the donor and acceptor side, respectively,45,46 as well as from competing dissipative recombination reactions.47 The average value of α attains a minimum of about 0.06, and it strongly depends on the pH48,49 and on the replacement of exchangeable protons with deuterons, thus illustrating the effects of hydrogen-bonding networks.47 The β parameter represents a “trivial” effect due to double charge separation in a single-turnover flash, depending on the duration of the flash.38 A detailed view of the Kok cycle is shown in the left-hand bottom part of Figure 1A, and it comprises the following types of processes: (i) reduction of P680+ by the tyrosine residue YZ of the polypeptide D1 (D1-Y161) and (ii) oxidation of the WOC by YZ• in a stepwise manner, resulting in the accumulation of four oxidizing equivalents. This is followed by the release of oxygen through an exergonic process, using water as the substrate. A comparison of the Kok cycle with the pattern of water oxidation in solution (see left side of the top panel of Figure 1A) reveals that the oxidation steps of the WOC are also accompanied by proton release, but the release pattern is different. The coupling of the electron transfer (ET) with proton transfer (PT) is known as proton-coupled electron transfer (PCET), and it is relevant to many redox processes, including water oxidation.16,50−55

wavelength of 700 nm has an energy of 1.77 eV) is apparently too low to provide the driving force to perform this process. The above considerations show that two prerequisites must be satisfied so that photosynthesis using the spectrum of visible light can be realized in living systems; these are (i) a light-induced reaction leading to a strong enough oxidant, and (ii) a catalytic system that governs the energy profile of the corresponding redox reactions by adjusting 4 equiv of a strong oxidant, leading to the splitting of two water molecules into O2 and four protons. The solution to this problem was brought about by photosynthetic organisms through an extensive period of evolution around 3 billion years ago.20−27 Evolutionary changes in these organisms included: (i) the development of a special protein matrix that enabled a substantial increase in the redox potential of the chlorophyll a (Chl a) molecule to about 1.2 V28 to serve as the “oxidant”, and (ii) the “construction” of a water-oxidizing complex (WOC) with an Mn4CaOx cluster acting as the catalytic site. (Note: The water-oxidizing complex is often designated with OEC. However, in enzymology, enzymes are named by their substrates; therefore, the term WOC seems to be more rational and will be used here.) To achieve this goal, the number of polypeptides increased to a surprisingly large extent as compared to the precursor reaction center (RC) of anoxygenic photosynthetic organisms unable to oxidize water.29 The final result of the evolutionary process was a multimeric complex called Photosystem II (PSII), which is located in the thylakoid membranes of all oxygenic photosynthetic organisms. With respect to the handling of the redox system 2H2O/O2 + 4H+ (see top panel of Figure 1A), nature has evolved two entirely different transition metal complexes to catalyze the highly endergonic reaction in the forward direction (i.e., the WOC of PSII) and the highly exergonic reaction in the backward direction (cytochrome c oxidase (COX) of the respiratory chain). Moreover, the WOC and COX both function in a unidirectional manner.30

2. REACTION MECHANISM OF WATER OXIDATION IN PSII The unique PSII complex in photosynthesis acts as a water, plastoquinone-oxidoreductase: 2PQ + 2H 2O(l) → 2PQH 2 + O2 (g)

(4)

The overall process in eq 4 comprises three types of reaction sequences:14,31 (i) Formation of the strongly oxidizing P680+ species induced by light illumination, resulting in charge separation (eq 5): Ant‐P680PheoQ A → 1[Ant‐P680]*PheoQ A → Ant‐P 680+Pheo−Q A → Ant‐P680+PheoQ A −

(5)

(ii) Water oxidation (eq 6): 4 ⊕ + 2H 2O(l) → O2 (g) + 4H+ Lumen

(6)

(iii) Reductive formation of plastoquinol (eq 7): 4Θ + 4H+Stroma + 2PQ → 2PQH 2

(7)

where Ant stands for the light-harvesting pigments (antennae) that harvest and transfer (using radiationless excitation energy transfer (EET)) the excitation energy to the RC pigments where the primary charge separation occurs. However, at the RC six chlorins (four Chl a and two pheophytin a molecules) form an excitonically coupled pigment complex so that the definition of 2888


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Figure 1. (A) The electron- and proton-transfer steps in the univalent redox sequence between 2H2O and O2 + 4H+ in aqueous solution (top panel) and the extended Kok scheme of photosynthesis (bottom panel). See text for details. Adapted with permission from ref 19. Copyright 2012 Elsevier. (B) Oxygen evolution as a function of the number of short flashes. A damped oscillation pattern with a period of four flashes is observed. Adapted with permission from ref 12. Copyright 2002 Springer.

3. ENERGETICS OF WATER OXIDATION

ΔG°(Si + 1/Si ) = ΔG°(P680+/P680) + ΔG°

Experimental differences in the standard Gibbs free energy values ΔG°(Si+1/Si) (Si and Si+1 are different redox states) can only be determined indirectly, as the absolute values of the energy levels of the Si states are not known. Early mechanistic and energetic studies suggested that the free energy gap ΔG°(Si+1/Si) is about 1 eV for i = 1, 2, and 3,56,57 whereas the value of ΔG°(S1/S0) may be significantly lower. More detailed estimations were performed on the basis of the relation (eq 8):

(P680YZ•Si /P680+YZSi ) + ΔG°(YZSi + 1/YZ•Si )

(8)

In this equation, ΔG°(P680 + /P680), ΔG°(P680Y Z • S i / P680+YZSi), and ΔG°(YZSi+1/YZ•Si) represent the Gibbs free energy differences for the formation of the cation radical P680+, the oxidation of YZ by P680+, and Si-state transitions, respectively. ΔG°(Si+1/Si) values of 1.10 (1.12), 1.15 (1.10), and 1.0 (1.08) eV were obtained for i = 1, 2, and 3, respectively; ΔG°(S1/S0) has been estimated to be 0.85 eV, which is lower than ΔG° for the other S-state transitions by 0.15−0.30 eV.58,59 2889


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Figure 2. (A) Schematic representation of the cofactor arrangement in the core of the reaction center (the view is along the membrane plane). Organic cofactors (for the sake of simplicity, the heme group of cytochrome b559 is omitted) are colored green (Chl), yellow (Pheo), magenta (plastoquinones QA and QB), and red (carotenoids). Ca (yellow), Fe (blue), and Mn (red) are shown as spheres; the figure was generated using PyMOL (http://www. pymol.org). The coordinating protein subunits D1 and D2 are indicated by dotted lines. Reprinted with permission from ref 19. Copyright 2012 Elsevier. (B) Structural arrangement of the Mn4CaOx cluster and its coordination sphere based on X-ray diffraction crystallography data.84 See text for the assignment of amino acid residues and water molecules (W1−W4) as ligands. Mn1, Mn2, Mn3, and Mn4 denote the different Mn ions of the WOC (see text for details). Reprinted with permission from ref 84. Copyright 2011 Nature publications. (C) Hydrogen bonds around (D1-Tyr161). The bonds between metal atoms and water ligands are depicted as solid lines, and the hydrogen bonds are depicted as dashed lines. Distances are expressed in angstroms. Reprinted with permission from ref 84. Copyright 2011 Nature publications.

experiments for any reliable energetic considerations to be made. Regardless of the exact quantitative numbers for ΔG°(S1/S0), an additional 0.3 eV in Gibbs free energy is gained in subsequent redox subprocesses. It is still unknown what the role of the energetic anomaly found for the YZ•S0 → YZS1 + n0H+ transition is. There is no experimental evidence for the existing speculations that this additional Gibbs free energy can be temporarily stored.69 The result of this particular energetic profile is that no S0 level is populated in samples that are dark-adapted. Moreover, this is most probably relevant with regard to possible deleterious reactions that are still not completely clarified.70 On the basis of the thermodynamics of the reaction, biological water splitting is allowed at pH values down to 5.0. This can be stated, even though experimental error does not allow for precise determination of the ΔG°(Si+1/Si) values (shaded areas in the right-hand bottom part of Figure 1A). The last stage of the oxidative water splitting is the exchange of the product with the substrate; this exchange was originally considered to be exergonic (by 0.1−0.2 eV).71 The elimination of UV-absorption changes by elevated O2 pressures (reflecting the turnover of YZ•S3)72,73 and the effect on delayed fluorescence led to the suggestion that the reaction sequence (eq 9):

These values show that, in comparison with the situation in aqueous solution, the reaction coordinate in water oxidation by the WOC of PSII in the four steps is energetically very well tuned.60 Of special relevance is the small driving force of about 0.1 eV (the reduction potential of P680 is about +1.25 V),61 which implies that the overpotential of the oxidation steps in the WOC for i = 1, 2, and 3 is extremely small. This stands in marked contrast to water oxidation performed by synthetic catalysts, driven either by electrolysis or by chemical oxidants; for example, the overpotential for O2 evolution on hematite photoanodes was determined to be 0.5−0.6 V.62 The minimization of overpotential is of importance in designing efficient synthetic catalysts for water oxidation; however, the mechanisms underlying the energetic tuning of the WOC remain to be unraveled in future studies. The situation is considerably different for the oxidation of the WOC in S0, where the Gibbs free energy gap between P680+YZS0 and P680YZS1 is about 0.4 eV. In this respect, the estimated value of 0.85 eV for ΔG°(S1/S0) (vide supra) is not in line with the determined redox potential of the redox-active tyrosine YD of polypeptide D2, which was reported to have a midpoint potential (Em(YD/YD•)) of about +0.75 V.63,64 This number is small as compared to the estimated Em of about +1.1 V for YZ/YZ•.44,65 Experimental data for tyrosine in synthetic model proteins66 are critical benchmarks for any reliable determination of ΔG°(S1/ S0), because YD• is known to oxidize S0 to S1 in both cyanobacteria49 and higher plants.48,67,68 Therefore, it is important to determine the value of Em(YD/YD•) by new

YZ•S3 ↔ [YZS2 (HxO2 )] ↔ [YZS0(O2 )] ↔ YZS0 + O2 + n3H+

(9)

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Figure 3. Top panel: PCET scheme. Bottom panel: Simplified reaction sequence (left side) and corresponding energetics (right side) for the reduction of P680+ by YZ in PSII with an intact WOC in the S1 state. The initial state I and the two relaxed states R,1 and R,2 are marked in red (I), green (R,1), and blue (R,2). See text for details. Reprinted with permission from ref 19. Copyright 2012 Elsevier.

dicted on the basis of fluorescence studies.76 Further, mass spectrometry77 studies clearly revealed that high O2 pressures do not limit the process of O2 evolution and that the ΔG° values are higher (by about 0.2 eV) than assumed previously.71

to be two different but intimately coupled cofactors. Accordingly, the reaction in eq 6 in fact comprises two distinctly different types of reactions: (i) the oxidation of YZ by P680+ and (ii) the stepwise oxidation of the WOC by YZ•.

4. COFACTOR ARRANGEMENT IN PSII The crystal structure of PSII, isolated from thermophilic cyanobacteria, was determined during the past decade by X-ray diffraction (XRD) crystallographic studies,78−83 and a resolution of 1.9 Å was achieved.84,85 Figure 2A shows the structural array of the cofactors that perform the reaction sequences of water oxidation in PSII shown in eqs 5−7, and Figure 2B presents a more detailed picture of the first coordination sphere of the catalytic Mn4CaOx cluster. (Note: The 1.9 Å XRD structure84 clearly shows a Mn4CaO5 core; in this Review, “x” is used instead of “5” to account for the possibility that the number of bridging O atoms may be different in the S3 and S4 states.) In Figure 2C, YZ and its immediate environment are shown. The reactions shown in eqs 5 and 7 are not the topic of this Review, and, therefore, only some relevant reviews and book chapters32,33,61,86−89 will be mentioned for reference and further reading. Two important features of the reaction sequence in eq 6, as revealed by the high-resolution XRD analysis of PSII, are (i) YZ, which was identified as Tyr 161 of polypeptide D1,43,44 is not part of the first or second coordination sphere of the Mn4CaOx cluster (the distance between Tyr 161 and Mn−Ca cluster is about 7.0 Å83,84), and (ii) YZ and the Mn4CaOx cluster are connected by a pronounced hydrogen-bonding network. On the basis of these properties, YZ and Mn4CaOx should be considered

5. OXIDATION OF YZ BY P680+ The reaction mechanism of P680+ reduction and the mechanism of YZ oxidation have been described in detail in several reviews and book chapters;16,90,91 therefore, only a brief summary will be presented here. The XRD structure determined at 1.9 Å resolution features a strong hydrogen bond between YZ and the ε-N atom of D1His190; two H2O molecules are also involved (Figure 2C). The water molecules seem to be important for the presence of a short contact involving the phenolic O atom in the reduced YZ and the ε-N atom in D1-His190; this is supported by quantummechanical computational studies.92 As shown in Figure 3, the oxidation of YZ by P680+ includes electron transfer from the tyrosine fragment to P680+ and is accompanied by proton transfer from the phenolic O atom of YZ to the His190 moiety. Such a process is called multiple-site proton and electron transfer (MS-PET). MS-PET is not unique to the reduction of P680+ by YZ, but is a feature common to a variety of redox reactions.51 In fully competent PSII complexes, the reduction of P680+ is efficiently coupled with the oxidation of YZ. The reduction of P680+ is characterized by multiexponential components, which are observed in all different types of PSII samples analyzed so far from cyanobacteria and higher plants with an intact 2891


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Figure 4. Photoassembly of the WOC. States A and F represent the initial and the final state of the reaction sequence, which comprises two light-driven reactions (A → B and C → D). These reactions lead to the oxidation of a MnII to a MnIII ion and an intermediary Ca-dependent dark reaction that gives rise to conformational changes, as indicated by the differently shaped symbols. State I is reached after light or UV-B stress104,119 and eventually leads to self-repair of the PSII complex.121,122

the mechanism of the process. The “fast ns” kinetics of the reduction of P680+ by YZ can apparently be well described using the theoretical value of the rate constant. In other words, this step is not affected by any triggered reaction or by the coupled proton transfer. This is supported by the lack of an isotope effect on the “fast ns” kinetics upon exchange of the protons with deuterons (kH/kD < 1.05107) observed with an intact WOC. Analysis of the XRD structure at 1.9 Å resolution shows the occurrence of mutual hydrogen-bonding interactions between YZ and the WOC, as depicted in Figure 2C.84 The hydrogenbonding scheme should differ for the redox states S0 and S1 in comparison with S2 and S3, as the latter bear an additional positive charge.108−113 Such changes in hydrogen bonding and the localization of the additional charge may cause the state P680YZ• in S0 and S1 to be energetically more favorable than the initial state (vide supra). This effect is characterized by values of 30−50 meV.97 In samples from which the WOC has been removed, the reaction coordinate of the reduction of P680+ by YZ undergoes significant changes. This corresponds to a substantial increase in the activation energy, by a factor of about 3, and to a kinetic H/D isotope effect of 2.7−3.3; this isotope effect is not present in the “fast ns” and “slow ns” kinetics in the intact PSII complexes.89

WOC.65,93−98 These kinetics can be approximated by three exponentials with half-life times of 20−50 ns (“fast ns” kinetics), 300−600 ns (“slow ns” kinetics), and 30−50 μs (“35 μs” kinetics), which are much faster than the 100−200 μs kinetics of the competing recombination reaction between P680+ and QA−.99,100 The multiphasic reaction mechanism of the reduction of P680+ by YZ is consistently explained by a model that is based on two assumptions:19,97 (i) the redox step is very fast (“fast ns” kinetics) and leads to an initial “quasi-equilibrium” [P680+YZ ↔ P680YZ•]I, described by the constant (Keq)I, and (ii) the relaxation process involves at least two different steps, one with a “slow ns” and the other one a “35 μs” kinetics, which may reflect changes in the hydrogen-bonding network. This should cause increases in the (Keq)relax values, thereby increasing the YZ• population. Thus, misses in the Si-state transitions of each single turnover in PSII47 are less probable. The left-hand panel of Figure 3 shows a description of the reaction system, as supported by experimental photoacoustic data.101 The right-hand panel includes typical energy data characterizing various stages of PSII with the WOC in the states S1 or S0. For the WOC in the states S2 and S3, the first step is even slightly endergonic. On the basis of these data, it can be concluded that, in general, the energetic profile of the process is determined by relaxation processes. This confirms the relevance of the protein matrix with regard to adjusting the reaction parameters. Moreover, it seems that the oxidation of YZ by P680+ has not changed over the course of evolution, as the multiphasic kinetics observed in cyanobacteria and in higher plants (vide supra) are rather similar. The activation energy of the “fast ns” reaction is in the order of 10 kJ/mol in both cyanobacteria and higher plants when the WOC attains the redox state S1.102 A reorganization energy of 0.6 ± 0.1 eV19,103,104 is applied in the assessment of the experimental rate constants and the activation energy. The edge-to-edge distance between P680+ and YZ was calculated to be 10 ± 1 Å,19 using an empirical formula involving the rate constant and distance.105 This is equal to the value of 9 ± 2 Å106 reported previously, and is also consistent with the edge-to-edge distance of the two species found in the high-resolution crystal structure.84 This perfect agreement between the predicted and experimentally estimated distances is important for the study of

6. ASSEMBLY, STRUCTURE, AND FUNCTION OF THE WOC For a thorough description of the function of the WOC, the following properties have to be elucidated in detail: (i) the formation and geometric structure of the Mn4CaOx core and its surroundings; (ii) the electronic structure and the arrangement of atoms in the active site in the different Si redox states of the Kok cycle; (iii) the kinetics of each Si-state transition; (iv) sites for substrate binding and product formation; and (v) the overall mechanism of the water-oxidation process. 6.1. Assembly and Decomposition of the WOC

The activity and stability of the WOC are characterized by a bellshaped pH dependence with a flat maximum around pH 6.5 and steep declines in the acidic (pH < 6.0) and alkaline (pH > 8.0) ranges.48,114,115 The WOC also has a comparatively high susceptibility to thermal decomposition.116,117 Exposure to UV-B radiation was shown to predominantly cause decom2892


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position of the WOC instead of other PSII components.118−120 A preferential susceptibility to visible light was also reported, which was proposed to lead to photoinhibition of PSII.121,122 To maintain photosynthetic activity under long-term illumination, the function of PSII has to be restored. This was shown to be achieved by a repair cycle involving the removal of the damaged D1 subunit from PSII, the synthesis of new D1, and its insertion into the damaged PSII.120,123 This way, the damaged PSII can be permanently restored as long as the organism is alive. After repair of the RC by insertion of a new D1 protein, the WOC has to be reassembled, which is a light-driven process called photoactivation.124−127 The formation of the Mn4CaOx core in the photoactivation process is highly exergonic.124−127 This assembly can be divided into two light-triggered reactions, between which a dark stabilization step occurs. The substitution of Mn with any other transition metal ion does not result in a functional WOC cluster. On the other hand, the redox-inert Ca2+ can be replaced with Sr2+ as a surrogate (see ref 128 for a structure of Srsubstituted PSII at 2.1 Å resolution) with a reduced activity.124−128 Figure 4 schematically illustrates the reaction sequence of photoactivation. The photoassembly of the Mn4CaOx cluster occurs via the oxidation of MnII to MnIII/ MnIV, with P680+ acting as an oxidant and YZ as an intermediary redox carrier. A suitable ligation of Mn requires the presence of Ca (or Sr). The kinetics of the reaction sequence of photoactivation have been resolved by measurements of the yields of the flash-induced production of oxygen in samples under reconstruction conditions.129,130 The assembly of the WOC cluster is the last stage in the formation of the photosynthetic apparatus in aerobic organisms.131,132 A maximum total turnover number (TON) of 105 is estimated for the WOC when one accounts for a repair cycle time of about 30 min.120 However, the WOC cluster is continuously repaired in the repair cycle.

Recently, a radiation damage-free structure of PSII at the S1 state was obtained at 1.95 Å resolution with a femtosecond X-ray free laser (XFEL).141 This was made possible by use of a large number of isomorphic, large PSII crystals and the femtosecond X-ray pulses provided by SACLA, Japan. The use of femtosecond XFEL enabled data collection before damage occurs (diffraction before destruction). The results showed that the Mn···Mn distances are shorter by 0.1−0.2 Å than those obtained from the high-resolution crystal structure analysis with the synchrotron radiation X-rays,84 and therefore the new data are consistent with those obtained with EXAFS studies.135,142,143 The Mn4CaOx core structure appears to be different for the redox states S0 and S1, whereas only minor changes were detected for the S1 → S2 transition. Pronounced changes in the arrangement of the nuclei were found in the S2 → S3 transition, as manifested by increases in the Mn···Mn distances from ∼2.70 to 2.82 and 2.95 Å.144 Similarly, for PSII complexes substituted with Sr, the Mn···Ca distances of 3.3−3.4 Å also decreased.145,146 The marked changes in the structure were also implied indirectly, for example, through differences in the reactivity of the S2 and S3 states toward NH2OH and NH2NH2147,148 and through Cabinding studies.149 QM/MM theoretical studies, with the support of XRD and spectroscopic experimental data, were employed to optimize the geometries of the Mn4CaOx complex in various redox states.137,138,150−153 However, the differences in the Mn···Mn distances between the XRD structure (and EXAFS results (vide infra)) and theoretical calculations are 0.1−0.3 Å in most cases; this falls in the experimental error range of the XRD analysis at the resolution of 1.9 Å.137,138,150−153 On the other hand, theoretical calculations showed that the new XFEL structure is mostly consistent with the S1 state structure,154−157 which also agrees with the results of simulation of roomtemperature EXAFS spectra.156 6.2.2. Coordination Sphere of the Mn4CaOx Cluster. The XRD structural data at 1.9 Å resolution unambiguously revealed the coordination environment of the Mn 4CaO x complex.84 As shown in Figure 2B, the coordination sphere of the Mn4CaOx complex contains, in addition to four water molecules, six carboxylate ligands (Asp170, Glu189, Glu333, Asp342, the C-terminus of Ala344 from polypeptide D1, and Glu354 of CP43) and one His (D1-His332) of the residues of the protein matrix. Several of these residues have been postulated on the basis of FTIR (Fourier transform infrared spectroscopy) data collected for mutated mesophilic cyanobacteria,134 except for Glu189 and His332 (both ligands coordinate to Mn1) and His337 (hydrogen-bonded to O3 rather than to Mn2). One striking feature of the first-sphere coordination environment is the bidentate coordination mode of the carboxylate groups of the residues D1-Asp170, D1-Glu333, D1-Asp342, D1-Ala344, and CP43-Glu354. The 1.9 Å XRD structure also reveals that all Mn ions are hexacoordinate.84,141 On the other hand, quantum-chemical DFT (density functional theory) studies favor a pentacoordinate Mn1 ion bonded to the His332 residue.151,152,158 The same conclusion was reached for the WOC S2 state by electron paramagnetic resonance/electron−nuclear double resonance (EPR/ENDOR) spectroscopic studies performed at low temperatures.150,158,159 X-ray spectroscopic studies on the mutant D1-H332E underline the crucial role of D1-His332.160 Hence, accurate information on the Mn1 coordination sphere is important for the elucidation of the mechanism; the structure of the Mn1 coordination sphere needs to be unambiguously

6.2. Structure and Function of the WOC

The structure of the WOC cluster is determined by (i) the arrangement of the four Mn ions, the bridging O atoms, and the Ca2+ ion; (ii) the first coordination environment of the Mn4CaOx core; (iii) the protein matrix surrounding the cluster; and (iv) the hydrogen-bonding network(s). The geometric structure of the WOC has been determined by high-resolution X-ray crystal structure analysis, and its electronic structure has been studied by extended X-ray absorption fine structure (EXAFS) and electron paramagnetic resonance (EPR). Complementary features of the ligand sphere were revealed by site-directed mutagenesis of individual amino acid residues.133,134 6.2.1. Structure of the Catalytic Mn4CaOx Cluster. The XRD structure at 1.9 Å resolution clearly revealed features of the Mn4CaOx core, such as bridging μ-oxo ligands and water molecules.84,85 As noted above, this structure might reflect a partially reduced S−i state, because the Mn atom is expected to be reduced below the dark-adapted state S1 by electrons generated by the exposure of the crystals to X-rays.135−138 In other words, the electron densities determined by the exposure of the crystals to X-rays are related to a Mn complex that may be reduced to near the MnII level, as suggested by an X-ray absorption spectroscopy (XAS) study on single crystals of PSII.135 It is possible that population of the S−3 state occurs,139 as this reduced state of the WOC is rather stable and can be obtained by reduction with NH2OH or NH2NH2.140 2893


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Table 1. Half-Life Times (t1/2 (μs)) of YZ• Reduction at 8−10 °C and of Si-State Oxidation at 20 °C in Spinacea oleracea and at 25 °C in T. vulcanus for the Reactions YZ•Si → YZSi+1−4δi3 + δi3O2 + niH+ (δi3 = 1 for i = 3; 0 for i ≠ 3) reaction:

YZ• reduction

species:

Spinacia oleracea

preparation temp i=0 i=1 i=2 i=3 a

thylakoidsa 8−10 °C 40−60 85 140 750

Si-state oxidation Spinacia oleracea PSII m.f.a 8−10 °C 70 110 180 1400

PSII m.f.b 20 °C 50 100 220 1300

T. vulcanus PSII corec 20 °C n.d.e 75 225 4100

PSII cored 25 °C n.d. 70 ∼130 1300

Reference 188. bReference 189. cReference 106. dReference 190. em.f. = membrane fragments; n.d. = not determined.

pulses produced at the Linac Coherent Light Source, for simultaneous XRD and X-ray emission spectroscopy (XES) of microcrystals of PSII at room temperature, were used to probe the protein environment and the electronic configuration of the Mn4CaOx cluster in the WOC. The XES data proved that the XRD data and the electron density correspond to PSII with a fully intact Mn4CaOx cluster and the configuration MnIII2MnIV2 in the S1 state.180 It was reported that a MnIIMnIIIMnIV2 configuration for the S0 state is rather unlikely.179 However, the S2 → S3 transition still needs to be studied in more detail, as it might involve either a metal-centered or a ligand-centered process.58 The electronic structure and nuclear arrangement of the S3 state are crucial for the mechanistic aspects of the formation of the O−O bond. A section on the mechanism of the water-oxidation process will be devoted to this topic. To achieve deeper insights into the metal-centered processes in the WOC, it has to be clear if the oxidation states are localized on individual Mn ions or delocalized over the cluster. Taking the EXAFS single-crystal structure of the Mn4CaOx complex in Thermosynechococcus elongatus181 as a starting model, the following was concluded with regard to the electronic configuration of the Si states:15 S0 = Mn1IIIMn2IIIMn3IVMn4III or S0 = Mn1IIIMn2IIIMn3IIIMn4IV, S1 = Mn1IIIMn2IIIMn3IVMn4IV, and S2 = Mn1IIIMn2IVMn3IVMn4IV (see Figure 2B for the numbering scheme for Mn). Nevertheless, t his is in disagreem ent with t he assignment o f Mn1IIIMn2IVMn3IVMn4III for the S1 state based on the recent damage-free XFEL structure.141,169 On the other hand, DFT calculations using the 1.9 Å XRD structure as a starting model led to the configuration Mn1IIIMn2IIIMn3IVMn4IV for the S1 state.182 Alternatively, X-ray resonant Raman scattering studies led to the conclusion that the electron removed from the Mn atom in the S1 → S2 transition may originate from a delocalized orbital.183 Currently, the type and extent of delocalization and the possible temperature dependence remain unknown. This is a crucial problem for the elucidation of the mechanism, because the WOC does not operate below specific threshold temperatures; this is closely related to protein dynamics, and more detailed studies are needed to clarify this issue. Recently, multifrequency, multidimensional magnetic resonance spectroscopy has shown that, immediately before the final oxygen-evolving step, all four Mn ions of the WOC are structurally and electronically similar, each having a formal oxidation state +IV and octahedral local geometry.184 Additionally, on the basis of femtosecond X-ray laser spectroscopy, it was suggested that the structure of the Mn4CaOx cluster becomes expanded in the later S state to bind the second substrate water molecule between the Mn4 atom and the rest of the cluster,185 although whether this kind of expansion indeed

confirmed, considering the possibility of structural changes during the Si transitions. In some papers,134,161−165 it has been proposed that only two Mn ions in the Mn4CaOx complex can change their oxidation states. This is expected if we adopt the “high oxidation state” model (see below); that is, the four Mn ions are in oxidation states of III, III, IV, IV in the S1 state, so that only the two Mn ions with a III valence can be oxidized from S1 to S3. The functionally most important ligands are the substrate water molecules; they provide the oxygen atoms for the eventual formation of O2. Earlier indirect lines of evidence, gathered from EPR spectroscopy166 and mass spectrometry,167,168 suggested the existence of a cluster of 6−12 water molecules in the WOC. The 1.9 Å resolution structure revealed four water molecules in the first coordination sphere of the Mn4CaOx cluster: two are bound to Ca and two to Mn4 (see Figure 2B).84,169 Additional water molecules are located between YZ and the WOC, and they form an extended hydrogen-bonding network. At present, it is not clear which of these water molecules contribute their oxygen atoms to the final O2 product (see ref 112 for a detailed discussion on the mechanism of O−O bond formation). FTIR difference spectroscopy170 can be employed to monitor the changes in ligand arrangement and hydrogen bonding over the course of the Kok cycle. The chemistry of water ligands bonded to the Mn4CaOx complex has been described on the basis of pronounced band shifts and negative bands in the 3588− 3617 and 3612−3634 cm−1 regions (characteristic for O−H stretching modes and in the region assigned to carboxylate stretching modes (1300−1600 cm−1)). On the basis of these data, at least four water ligands should be present.171 As a final point in this section, attenuated total reflection FTIR spectroscopy revealed that the orientation of the carboxylate group of CP43-Glu354 changes by 8° during the S1 → S2 transition as a result of a change in the coordination mode of the carboxylate (from bridging two Mn ions in the S1 state to chelating one Mn ion in the S2 state).172 6.2.3. Electronic Structure and Nuclear Arrangement for the Si States of the Catalytic Site. The electronic structure of the Mn4CaOx complex can be investigated by many spectroscopic techniques, such as XANES (X-ray absorption near-edge structure),55Mn ENDOR, EPR spectroscopy, and other methods.58,172−177 Although many studies have been performed, the overall oxidation state of Mn in the Mn4CaOx core is still the subject of controversy.178 It is widely postulated, on the basis of EPR and ENDOR results, that Mn in the S2 state bears the MnIIIMnIV3 configuration,179 with according ramifications for the other Si states. Such an “overall high oxidation state” model has been questioned178 and an “overall low oxidation state” description was introduced instead, in which the S2 state corresponds to MnIII3MnIV. Recently, intense femtosecond X-ray 2894


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Table 2. 18O Exchange Rate Constants from Thylakoid Membranes at 10 °C205 phase of exchange S0 state −1

fast, kf (s ) slow, ks (s−1) a

a

n.d. 13.6 ± 1.4

S1 state

S2 state

S3 state

n.d. 0.022 ± 0.001

118.8 ± 3.6 1.96 ± 0.12

37.5 ± 1.6 2.02 ± 0.06

n.d.: not determined.

A proteinaceous shield protects the Mn4CaOx complex against the process of dissipative reduction of the higher oxidation states S2 and S3. In all O2-evolving PSII, several extrinsic proteins form a barrier against the aqueous lumenal phase.201−204 Hence, there is a need to investigate the substrate/product pathways. Studies on H216O/H218O replacement provided the exchange rates of the water substrate in various Si states. The presence of two different water ligands was confirmed by the detection of biphasic kinetics involving Si-state-dependent rate constants.205 Examples of kinetic results are collected in Table 2. Recently, it was shown that the substrate/water exchange is dramatically slower in the transient S3YZ• state than in the earlier S states.206 These data show that the rate constants for the slow waterexchange process are at least 1 order of magnitude lower than those for the electron-transport chain, the latter being the ratelimiting stage.133 Therefore, the H216O/H218O turnover neither reflects the kinetics of substrate transport nor the rapid substrate/product replacement reaction M0L0W4 + 2H2O ↔ M0L0W0 + O2 + n4H+ (where M0L0W4 and M0L0W0 correspond to a transitioning S4 and final S0, respectively, and the subscripts depict the oxidation state of the manganese (M), the nonsubstrate ligand(s) (L), and the substrate water (W); for a discussion of this nomenclature, see ref 193). Instead, it points to relatively slow exchange reactions involving water ligands around the Mn4CaOx cluster and bulk water molecules in the intermediary redox states S0, S1, S2, and S3. This state of equilibrium may be influenced by the hydrogen-bonding scheme. Thus, the decrease in these exchange rates upon the abstraction of the spinach PSII extrinsic proteins PsbP and PsbQ can be explained.205,206 The transport of water substrate to the active site was estimated to take up to several milliseconds, as determined in studies of the interaction of the Mn4CaOx complex with small hydrophilic reductants, such as hydroxylamine or hydrazine.148 This way, preconditions that enable high rates of oxygen evolution can be fulfilled under continuous saturating illumination. Although the product concentration seems to be low, in the order of 250 μM in air-saturated water at room temperature, the substrate concentration in the water-oxidation process is very high. The opposite holds for cytochrome c oxidase, which catalyzes the reverse process (reduction of oxygen to water, coupled with a proton pump, at a dinuclear heme a3-CuB site, also embedded in a protein matrix):30 a high product concentration comes with a low substrate concentration. Thus, it is useful to compare the substrate/product transport modes in these enzymes.207 Putative channels for the transport of oxygen to the cytochrome c oxidase dinuclear active site have been identified,208 and analogous routes were expected to be present in the WOC for O2 evolution.31,209 Crystallographic data recorded for cytochrome oxidase ba3 from Thermus thermophilus with bound Kr/Xe atoms revealed the presence of a Y-shaped channel lined by hydrophobic amino acids, starting at the protein surface and ending at the active dinuclear heme a3-CuB center.

occurs remains to be verified by high-resolution crystal structural analysis of the higher S states. 6.2.4. Kinetic Aspects of the Water-Oxidation Process. Kinetic aspects of single-oxidation steps in the WOC and of the accompanying reduction of YZ• have been investigated by timeresolved flash-induced UV-absorption-edge measurements186 and EPR spectroscopy,187,188 respectively. The results are summarized in Table 1. The reactions YZ•Si → YZSi+1 + niH+ (i = 0, 1, 2) display essentially monoexponential kinetics, characterized by half-life times of 50−100 and ca. 200 μs for i = 1 and 2, respectively. For the process with i = 0, values of 50 and 250 μs were published.186,191 A more trustworthy value seems to be 250 μs, which has been confirmed by new FTIR results.192 Quite contrary to these processes, the kinetics of the reaction YZ•S3 → → → YZS0 + n3H+ + O2 appear to be more complex. The reaction has a sigmoidal time course and contains a lag phase that was interpreted to reflect proton release preceding the electron transfer from the Mn4CaOx cluster to YZ•.186 Nevertheless, experimental obstacles have prevented the acquisition of detailed insights into the lag phase: in studies on flash-induced absorption changes, misses and double hits are inherent problems,35 and they cause overlap of absorption changes in various Si-state transitions.193 On the basis of kinetic studies of the YZ• reduction process, monitored with EPR spectroscopy and by polarographic detection of oxygen evolution, it was concluded that the lag phase should not persist for more than 50 μs in vivo; this time limit may be extended in some cases.194 On the other hand, the extent of this phase seems to depend strongly on the pH.195 A thorough study of flash-induced transient FTIR changes helped to reveal more facts about the nature of the lag phase, and it showed important roles for deprotonation and protein relaxation.192 It is suggested that the lag phase reflects the triggered reactions present for all Si-state transitions. Moreover, as compared to other WOC redox steps, the general rate of YZ• reduction by the S3-state WOC is slower by a factor of 5−50. Its half-life time is also much more dependent on factors such as the mode of sample preparation,106 mutagenic specific replacement of the Asp61 residue in polypeptide D1 with other amino acids,196,197 substitution of Cl− with I− ions,198 and contact with phospholipase A2.199 Interestingly, on the basis of kinetic data (rate constants or activation energies using different PSII preparations), it was shown that the reaction coordinate has not changed during the evolution of ancient prokaryotic cyanobacteria into higher plants.200 6.2.5. Substrate/Product Pathways. PQH2 reoxidation occurring at the cytochrome b6 f complex, taking place with a rate constant of 10 ms−1, forms the rate-limiting stage in the linear electron-transport chain.133 Nevertheless, high TONs, observed for water oxidation by the Mn4CaOx complex upon irradiation with bright sunlight, need both kinetically fast redox transitions and fast enough consumption of the reagent water molecules and the accompanying evolution of the O2 and 4H+ products. 2895


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Luna et al.210 used these data to postulate a concerted sequence of transfer steps in which the water molecule at the catalytic site is repelled by the hydrophobic part of the oxygen channel. Most likely, rearrangements or motions of proteins are necessary to allow for optimum transport of the substrate to the catalytic site. This mechanism of feeding the active site with substrate might be helpful in the adaptation to surroundings with differing saturation levels of oxygen.210 On the contrary, release of the O2 product from the PSII active site may require fast substrate/ product exchange and a decrease in the probability of the formation of 1ΔgO2 by preventing O2 from coming in contact with the 3P680 state, which is populated through P680+QA− recombination.120,211 It remains to be investigated if the O2 transport route(s) contribute(s) to the irreversible catalytic water oxidation in the WOC.14,31 Protons are also products of the water-oxidation process. The proton-release scheme shows features that allow the assumptions that the S0/S2 oxidation processes lead to one proton abstraction, that the S1 oxidation involves no deprotonation, and that the reaction sequence of the terminal oxidation of S3 by YZ evolves oxygen and two protons (ni = 1, 0, 1, and 2 for i = 0, 1, 2, and 3, respectively).212 Electron transfer involving redox groups surrounded by a protein matrix with protonable groups may result in proton release with a noninteger stoichiometry, as shown for the S-state cycle in Figure 1A. For this example, the abstraction of protons seems to be blurred by transient, changing, and electrostatically triggered proton-transfer reactions.213−215 Protons thus produced at the active site are likely to be directed through the Asp61 residue of the polypeptide D183,216,217 into a route that includes the extrinsic PsbO protein. The uncommon results obtained in the titration of soluble PsbO may correspond to the involvement of Glu and Asp amino acids (present in this protein) in the H+-release route into the lumen compartment.218 Earlier detailed studies also support this postulate.219 Reports on higher-resolution XRD structures paved new ways for computational studies, which also covered substrate/producttransporting channels.220−223 The reported results lead to the conclusion that, most probably, there are different routes for substrate consumption and product release in the WOC. A model describing the possible channels for water, oxygen, and protons is illustrated in Figure 5.

Additional data on the transport of oxygen through channels were collected by Fourier transform ion cyclotron resonance mass spectrometry measurements for the oxidation of amino acids in the RC subunits D1, D2, CP43, and CP47. These data were compared to the results obtained from theoretical modeling of the channels, taking the XRD structure as a starting model. Thus, the possible meaning of dynamic processes in the protein matrix for the transport of water and oxygen has been underlined.224 Multiple-steered molecular dynamics, employed in computational studies, allowed for the description of the dynamics of water transport to the Mn4CaOx complex. It was assumed that water can access the active site in a controlled manner, avoiding harmful events that possibly lead to a loss of Cl− and/or Ca2+ ions. The transport rate was estimated to be 5000 H2O/s.225 On the basis of these results, it can be concluded that the transport of a substrate is fast enough to overcome any kinetic limitations in the case of steady-state turnover by the WOC under saturating irradiation. 6.2.6. Mechanistic Aspects of the Water-Oxidation Process. Some important mechanistic aspects of the WOC redox processes were elucidated by comparing the experimenexp tally determined rate constants ki+1,i in Si-state transitions with NET their “theoretical” equivalents ki+1,i . The latter were obtained by taking the 1.9 Å XRD structure as a starting model, applying the empirical rate constant−distance relationship provided in eq 10:105 log ki NET = 13 − (1.2 − 0.8ρ)(RDA − 3.6) + 1, i − 3.1(ΔGi0+ 1, i + λi + 1, i)2 /λi + 1, i

(10)

In this equation, RDA is the edge-to-edge distance between the reactants, ρ denotes the packing density of the protein atoms between the redox centers (ρ varies between 0 for vacuum and 1 for full package), ΔG0i+1,i is the Gibbs free energy gap between YZ/ YZ• and Si/Si+1, and λi+1,i is the reorganization energy of the reaction. NET Analyses of these data underlined that kexp i+1,i and ki+1,i differ 19,226 substantially, by more than 2 orders of magnitude. Such differences unambiguously confirm that electron transfer does not play a role in the rate-limiting stage in the Si-state transitions reaching S3. Therefore, one needs to apply the description of a sequential reaction of the type shown in eq 11: kitrigg + 1, i

kiNET + 1, i

YZ•Si ⎯⎯⎯⎯→ (YZ•Si )* ⎯⎯⎯⎯→ YZSi + 1 + niH+

(11)

for i = 0, 1, and 2. In this equation, ktrigg i+1,i denotes the rate constant of a triggering process preceding the electron-transfer stage and NET kinetically limiting the overall process (ktrigg i+1,i ≪ ki+1,i ), and • (YZ Si)* is a “triggered” Si state. In contrast to the observed monoexponential kinetic profile corresponding to the rate-limiting trigger reactions in the sequence of eq 11, a sigmoidal curve is detected for the time course of YZ• reduction by the S3-state WOC, and the general rate changes under varying conditions. Such behavior may be illustrated with the simplified reaction sequence denoted in eq 12: k 3trigg *,3

k4,3

YZ•S3 ⎯⎯⎯→ (YZ•S3)* ⎯→ ⎯ YZ[S2 (HxO2 )*]

Figure 5. Possible trajectories of the substrate/product channels between the Mn4CaOx cluster and the lumen. Thick, colored arrows indicate the suggested paths for water supply (blue), oxygen removal (pink), and proton removal (yellow).223 Reprinted with permission from ref 223. Copyright 2009 Elsevier.

→ → → YZS0 + O2 (g) + n3H+(aq)

(12)

where [S2(HxO2)*] corresponds to the coordinated S4-state peroxide and n3 to the overall H+ release, not considering any 2896


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(YZ•Si)* is very low; hence, the corresponding triggered states cannot be detected experimentally.114 It is assumed that there is at least one breakpoint in the reaction coordinate of the trigger process(es), as blockage of the sequences of eqs 11 and 12 for the Si-state transitions is observed below threshold temperatures.190,231,233 The QA− → QB electron transfer taking place at the PSII acceptor side, also in the case of anaerobic purple bacteria, shows a similar blockage upon freezing. The influence of the latter reaction correlates well with the protein dynamics, as was shown by Mößbauer spectroscopy234 and neutron scattering.235 Figure 7 presents a

single deprotonation step(s). Moreover, the last steps, leading to oxygen coordination to form [S0(O2)*] and to water/oxygen exchange (see eq 9), are omitted for clarity; the back-reactions are also not explicitly represented. Considering that the time courses for YZ• reduction by the S3state WOC and oxygen evolution are similar, two different types of rate limitation in the sequence of eq 12 can be distinguished:194,227−229 (i) the rate of the trigger reaction is low in comparison with that/those of the redox reaction(s) and forms a sequence involving at least two steps, with the sigmoidal time course as a consequence; and (ii) a “fast” trigger reaction (with a time constant resembling that of the other Si transitions) occurs with subsequent general electron transfer at a lower rate, which is affected by its involvement in a fast unfavorable redox equilibrium with a low Keq. These two models cannot be resolved in a straightforward manner because of the lack of available timeresolved FTIR data.192 Nevertheless, the second option seems more attractive; therefore, the kinetics of YZ• reduction and oxygen evolution have been simulated for this model.19 Despite the information on the mechanism contained in the sequences of eqs 11 and 12, as illustrated in Figure 6, there is a

Figure 7. Temperature dependence of the average atomic mean square displacement ⟨u2⟩ for the hydrated (full symbols) and dry PSII membrane fragments (open symbols). The temperature ranges of different mobility characteristics are separated by dashed lines. The thermal blockage of S1 oxidation and of S0, S2, and S3 reactions is marked by yellow and green areas, respectively. The electron-transfer efficiency data are for the electron transfer from QA− to QB.235 See text for further details. Reprinted with permission from ref 19. Copyright 2012 Elsevier.

comparison between the temperature dependence of the protein dynamics and that of the thermal blockage of both transitions involving the Si states, as well as the reoxidation of QA− by QB within the membrane fragments of PSII. The results led to the conclusion that all processes, excluding the S1 → S2 transition, are strictly dependent on protein dynamics.19,235 The origin of the significantly lower threshold temperature of the S1 → S2 transition than those of the redox steps of the other Si-state transitions is that, most probably, there are differences in the deprotonation scheme. In contrast to the former reaction, the latter reactions are coupled with substantial releases of protons into the lumen part.212 Such a property leads to the conclusion that the mode of proton shifts in the hydrogen-bonding system involving YZ and the Mn4CaOx complex, as shown in Figure 2C, is crucial for the WOC trigger reactions. For the S1 → S2

Figure 6. Kok cycle for water oxidation driven by P680+, with YZ acting as an intermediate and the Si states in their transient, triggered conformation (symbolized by a star). See text for further details. Adapted with permission from ref 19. Copyright 2012 Elsevier.

need to extend the conventional view of the Kok cycle. There are NET two crucial implications of the ktrigg i+1,i ≪ ki+1,i relation: (i) experimentally investigated features of kexp , such as activation i+1,i energies, thermal blockage (as denoted in Table 3), or kinetic isotope effects, correspond to the profile of the trigger reaction(s) for i = 0, 1, and 2, rather than that of the redox step; and (ii) the probability of population of the transient state

Table 3. Activation Energies (Ea (kJ/mol)) and Threshold Temperature for 50% Blockage (ϑ1/2 (°C)) by Freezing of the Reactions YZ•Si → YZSi+1−4δi3 + δi3O2 + niH+ (δi3 = 1 for i = 3; 0 for i ≠ 3) T. vulcanus

species: preparation:

PSII core Ea (kJ/mol)a

i=0 i=1 i=2 i=3

Spinacia oleracea

n.d. 9.6 26.8 15.5/59.4f

PSII membrane fragments ϑ1/2 (°C)a n.d. ∼ −90 ∼ −16 ∼ −10

PSII core

EA (kJ/mol)b

ϑ1/2 (°C)c

EA (kJ/mol)d

ϑ1/2 (°C)e

5 12.0 36.0 20.0/46.0f

∼ −50 ∼ −135 ∼ −45 ∼ −40

g

n.d. ∼ −100 ∼ −50 n.d.

n.d. 14.8 35.0 21.0/67.0f

a Reference 190. bReference 189. cReferences 19, 230, and 231. dReference 106. eReference 232. fThe two values for i = 3 were determined from the Arrhenius plots with breakpoints (above/below55). Values from reports without a breakpoint phenomenon are about 30 kJ/mol.228 gn.d. = not determined.

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transition, a thermal threshold is still observed, whereas no such observation is made for the charge separation that results in the presence of the ion-radical pair P680+QA−236 or for its dark recombination,237 which is limited by the electron-transfer rate. The nature of the triggering reactions at the acceptor and donor sides of PSII remains unknown. It is postulated that structural changes in the surroundings of the cofactors (e.g., in the hydrogen-bonding scheme) enable the redox reactions, including water oxidation, to occur at low overpotentials. This assumption still needs clarification, which is a challenge for future research. At the same time, an important fact in the oxidation of two water molecules (to form oxygen) is the formation of a covalent bond between two O atoms; hence, mechanistic aspects are a hot research topic.169 The energetic balance may lead to the conclusion that the O−O bond is formed as a result of the population of the coordinated peroxide, which is an intermediate in photosynthetic water oxidation.56,71 This assumption of a peroxidic transient state seems to be appropriate, as shown with several quantum-chemical computational studies and with experimental data for model complexes of ruthenium that are active in water oxidation.238,239 Nevertheless, the majority of peroxidic compounds in the water-oxidation process catalyzed by ruthenium contain a terminal peroxide moiety bonded to a Ru atom.238,239 The original model assumes that the formation of such intermediates corresponds to the state S3. Such a hypothesis, however, is not taken into consideration in the vast majority of currently discussed schemes, which all have a coordinated peroxide as an intermediate (either mononuclearly or dinuclearly coordinated), but they assume that this state is exclusively formed in the S4 state.216 Three essentially different models with regard to the nature of S3 and its reaction with YZ• are currently discussed, as schematically illustrated in Figure 8. The S4-based models assume that S3 attains a single electronic configuration and nuclear geometry, either of the form S3(W) = M3L0W0, corresponding to the “Mn only” model (A), or of the form S3(O) = M2(LW)1, called the “oxo-radical” model (B). The oxidation of S3(W)/S3(O), induced by YZ•, is postulated to lead to the formation of a coordinated peroxide (S4(P) = M2L0W2); subsequent steps result in oxygen evolution. As an alternative, a “multiple S3 state” model (C) was considered by some groups60 in which two postulates are made: (i) the S3-state contains a mixture of Mn4CaOx complexes differing in electronic structure and nuclear arrangement (S3(W) = M3L0W0, S3(O) = M2(LW)1, and S3(P) = M1L0W2); these complexes are in equilibrium within a few milliseconds or even faster; and (ii) oxidation of S3 by YZ• induces a configuration S3(P) = M1L0W2 for a coordinated peroxide, which leads to further steps that involve the transient population of the S4 state, as illustrated in Figure 8. Kinetic studies showed that the probability of the population of S3(P) is low (less than 5%); hence, there are difficulties in the detection of this state.213 Taking the “multiple S3 state” model into consideration, the WOC should be blocked in the process of oxygen evolution to prevent the population of S3(P). This clearly explains the marked heterogeneity of PSII for the activity of S3 in the CP43-Glu354 mutant of Synechocystis sp. PCC 6803.240,241 The formation of M1L0W2 was assumed to strictly depend on a proton shift to establish an equilibrium between the tautomeric forms.60,194 This allows us to postulate that, upon substituting a Glu residue with a Gln residue at site 354 of CP43, the proton shift(s), necessary for the S3 form of the M1L0W2 population, is/are interrupted in

Figure 8. Schematic representation of the “Mn only” model (A), the “oxo” model (B), and the “S3 multistate” model (C) (top panel) and the redox isomerism equilibrium and proton tautomerism models (bottom panel). The superscript c refers to the complexed peroxidic state and x indicates the unknown protonation state. The presented Mn valence state corresponds to the widely accepted “high-valence Mn” model (see text for details). Reprinted with permission from ref 19. Copyright 2012 Elsevier.

many PSII complexes. The theory involving tautomeric equilibria was published by Kusunoki for the WOC in other states.242,243 Current studies on the mechanism of the formation of the O− O bond in the WOC are mainly performed by calculations based on XRD structural data. Within the framework of the “overall high oxidation state” model, the state M3L0W0 of model A (see Figure 8) corresponds to the electronic configuration MnVMnIV3. An oxomanganese(V) group (MnVO) may be the site of the formation of the O−O bond via nucleophilic attack by a substrate molecule.216−251 Complexes containing a MnVO group have been synthesized, and their properties have been analyzed.248−250 Evidence was presented that the formation of the O−O bond can occur through nucleophilic attack of the hydroxide ion on the oxo ligand of the MnVO moiety.248 It was reported that the MnIV−O• (oxyl) is more favorable than the MnVO moiety as an intermediate for water oxidation. Thus, a rearrangement or tautomerism is possible for the MnIV−O• (oxyl) and MnVO moieties.250 In other words, theoretical analyses revealed that the activation energy for this type of reaction is too high to take place in the WOC and that, instead, an oxo-radical bound to MnIV is the most likely reactant from a theoretical viewpoint.151,157,216,251 These studies suggest that two oxo radicals in S4, including at least one bridging oxo group 2898


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increasing knowledge of how the WOC operates in nature. With this in mind, we now summarize several attributes of photosynthetic water oxidation that should be considered when designing a synthetic catalyst.

of the Mn4CaOx cluster, are linked together to obtain a peroxide dinuclearly coordinated by two Mn atoms.151,157,251 However, alternatively, DFT calculations led to the conclusion252 that the formation of the covalent O−O linkage can already take place in S3, with the electronic configuration Mn1IIIMn2IVMn3IVMn4IV− O•H, which is transformed into the peroxidic configuration Mn1IIIMn2IIIMn3IVMn4III−O−OHCa. In this case, the peroxide is dinuclearly coordinated to Mn4 and Ca. The oxidation of this state by YZ• was inferred to eventually lead to ground-state triplet O2 via the transient formation of a coordinated superoxide.252 However, some estimates suggest that such an oxyl state is energetically inaccessible, based on the work on model compounds.254,255 Another important factor for the discussion of the mechanism of the O−O bond formation is the role of protons and the protein surroundings. In previous studies, the influence of proton-accepting groups on the energetic aspects of water oxidation was described.253 A variety of results concerning the functionally important protonation mode in the reverse process (O−O bond cleavage in oxygen enzymology256−259 and model systems260,261) are available. Hence, it is assumed that similar effects may play a role for the chemical formation of the O−O bond.193 This is confirmed by DFT calculations performed for the dinuclear Ru complex that is known as the “blue dimer”, which reveal that the formation of the O−O bond is accompanied by several proton-transfer steps.239 Similarly, quantum-chemical studies showed that proton transfer also occurs when the process involves a mononuclear Ru complex as the reagent.262 Currently, no specific data are available for the hydrogen bonding in the S3 state (see section 5 for the process of oxidation of YZ by P680+). Analogously, it has not been revealed how the proton-transfer steps are involved. Consequently, two assumptions are made in an only general discussion on the role of protons: (i) in the S3 state, the crucial agent for the formation of the O−O bond is the local proton gradient ∇H+(r,⃗ t,S3) in the vicinity of the reacting O atoms; and (ii) the dependence on the space vector r ⃗ governs the probability of the population of the three S3 redox-state configurations (M3L0W0, M2(LW)1, and M1(LW)2) and the time profile, due to the hydrogen-bonding dynamics that modify the quickly established equilibrium of these S3-state electronic configurations. Apart from the effects of ∇H+(r,⃗ t,S3), structural modifications of the ligand may also change the orientation of the Mn redoxactive orbital, modifying its activity by some orders of magnitude. Reference 263 contains a review of the impact of ligand fields on the properties of metal−oxo complexes. This effect is illustrated by the influence of the reorientation of a Glu residue on the activity of the dinuclear nonheme Fe ion that is included in the catalytic site of some oxygenases; the Glu reorientation involves the binding of a “regulator” protein.264 Although some experimental details are missing, it can be stated that dynamic and flexible proteins do tune the scalar proton H+(r,⃗ t) around the Mn4CaOx complex and YZ• in all Si states. Thus, the impact of protein dynamics and the flexibility of the functional WOC system can be explained, as shown by the thermal blockage of the Si-state transitions at temperatures below a certain threshold (vide supra). Similarly, a lower extent of hydration of the sample results in inhibition of the processes at low temperatures.265

7.1. Mnn+ and Ca2+: Abundant and Environmentally Friendly Ions

While nature uses the abundant metal ions Mnn+ and Ca2+ for water oxidation (Figure 9), many other metal-based catalysts also

Figure 9. Abundance (atom fraction) of the elements in Earth’s upper crust as a function of the atomic number. Image from http://pubs.usgs. gov/fs/2002/fs087-02/. A more detailed caption can also be viewed at this site.

show promise for water oxidation under various conditions; however, the use of these often rare and expensive elements or compounds on a global scale is problematic because of concerns about their toxicity, high cost, and limited availability.266 The natural WOC, by comparison, shows that an appropriate arrangement of Mn and Ca ions will form a highly efficient catalyst for photoinduced water splitting, and thus it should also be possible to use Mn or other environmentally friendly metal ions in water-oxidizing catalysts for artificial photosynthesis by adopting the strategies used by nature. The first-row transition metal ions, such as Mn, have low crystal field activation energies for oxidation-state changes during water oxidation as compared to the second- or third-row transition metal ions.267 On the other hand, the lifetime of radical species is also important in the oxygen evolution reaction.268 7.2. A Heterogeneous or a Homogeneous Catalyst

It is likely that heterogeneous water-oxidizing catalysts are more appropriate than homogeneous catalysts for use in artificial photosynthetic systems. Heterogeneity has the potential for increasing the robustness of the catalyst. The interaction of two separate Mn-based catalysts is low in situ, and it reduces decomposition, decoordination, or disproportionation reactions. The recovery of heterogeneous catalysts is also typically easy and cheap. However, the future catalysts may combine the benefits of homogeneous and heterogeneous catalysis.269 7.3. Tetranuclear Mn Structure for the WOC in PSII

7. LESSONS LEARNED FROM THE WOC TO ASSIST ARTIFICIAL WATER OXIDATION Biomimetic approaches for designing nanoscale devices that are capable of water oxidation require the application of our

The requirement to extract four electrons in the water-oxidation process poses chemical obstacles when only 1−2 Mn ions are involved, as each catalytically active Mn ion favors minimal changes to its oxidation state. The adoption of metal clusters is a 2899


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an elaborate protein framework may be not necessary for artificial catalysts because other strategies, such as polymer electrolyte membrane electrolyzers, work quite well.

common strategy used by nature to catalyze multielectrontransfer reactions. The clusters can simultaneously host, accumulate, and transfer many electrons to the reagents. Usually, tetra- and polynuclear metal oxides assist the four-electron wateroxidation process, making them good functional models for the WOC.270 Thus, as nature uses a tetranuclear Mn cluster to oxidize water, tetra- and polynuclear metal compounds are more promising catalysts for multioxidation or reduction reactions.270

7.7. Spin-Flipping Theory in Chemical Reactions

Spin-flipping processes often have high activation energies, as predicted by the spin-balance theory or the spin-balance rule.281−284 The application of this theory to water oxidation means that the directions of the spins on the WOC should be regulated carefully:

7.4. The pH Issue in the Water-Oxidation Reaction

Biological water splitting is performed at pH 5−6.5.271−273 However, in many artificial models (Mn complexes) for the WOC, degradation, disproportionation, and ligand-removal processes are observed at higher and lower pH values.274 Moderate pH conditions used by nature are more promising for the metal-based complexes, at least regarding the decomposition issue.

2H 2O(l) + [Mn4CaOx cluster (S4 )] → O2 (g) ↑↓

↑↑

↑ +

+ [Mn4CaOx cluster (S0)] + 4H (aq) ↓

(13)

The arrows in eq 13 show the spins of the electrons. Siegbahn suggested that this requirement can only be fulfilled if there are two Mn atoms directly involved (direct coupling). One Mn atom holds the oxygen radical and another Mn atom is being reduced in the O−O bond-formation process, for which antiferromagnetic coupling between the Mn spins is required (Figure 11).285 This type of smooth mechanism is not possible if

7.5. Proton-Coupled Electron Transfer in Biological Water Oxidation

Electron transfer not accompanied by the removal of a proton increases the positive charge of the Mn−Ca complex,51 which may result in an increase in its redox potential and in side reactions involving a highly oxidized cluster. To avoid highly charged species, the natural system uses PCET mechanisms.16,51,275 Such PCET processes have been reported for artificial water-oxidizing models (see Figure 10 for several examples).276−279

Figure 11. Proposed mechanisms for the O−O bond formation and spin states in PSII: (A) the direct coupling mechanism and (B) the water attack mechanism. Reprinted with permission from ref 285. Copyright 2010 American Chemical Society. Figure 10. Potential PCET mechanisms for the molecular model cobalt oxide cubane. It is noted that the charge is delocalized throughout the cube; the depiction of CoIII centers (red) and the CoIV center (blue) is solely for illustrative purposes. At pH < 3.1, the protonated form of the cubane (1-H+) is the stable species. At pH > 3.1, the cubane is deprotonated and 1 is the stable species. Reprinted with permission from ref 276. Copyright 2011 American Chemical Society.

only one Mn atom were involved, such as in the potential alternative mechanism in which the oxygen radical is attacked by external water molecules.285 As illustrated in Figure 11A, the low energy barrier for the direct-coupling mechanism is caused by the preference of Mn to be in a high-spin electron configuration. In the O−O bond-formation process, the second Mn4+ ion acquires a down-spin electron. Thus, an electron transfer without a change of spin can occur, and no spin-crossing should take place upon the formation of peroxide as the closed-shell product (Figure 11A). In the case of the water-attack mechanism, illustrated in Figure 11B, there is no such possibility; therefore, a spin-crossing is required, which leads to a high barrier (see ref 285 for details). The spin-crossing argument is similar to the Woodward−Hoffmann rules for orbital crossing in organic chemistry, but here it is applied for spin considerations.286 Careful design of the artificial models for water oxidation using quantum-chemical calculations to obey the spin-balance rule is a very promising strategy to introduce efficient catalysts.

Mimicking the strategy used by nature to place hydrogenacceptor groups around the active sites may find use in artificial models. 7.6. Channels in PSII

Oxygen and protons are rapidly produced in PSII. Thus, channels exist in PSII that transfer these compounds out of the reaction site and that transport substrate water to the reaction site by making use of electrostatic, structural, and orientational properties (Figure 5).223,280 In a highly efficient water-oxidizing compound for artificial photosynthetic systems, such channels are necessary around the active sites to keep them free from exposure to high concentrations of protons or oxygen. However, 2900


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resulting in a hydroperoxide ligand bonded to Mn.244 In the postulated mechanism, the Ca2+ ion acts as a weak Lewis acid.307 On the other hand, it already has been reported that, in this process, a water ligand bonded to Ca2+ interacts with a MnVO moiety to result in the evolution of oxygen through a nucleophilic attack. This mechanism has been further elaborated by Brudvig and co-workers.296,307,308 Recently, it was shown by X-band and Q-band EPR and 55 Mn ENDOR spectroscopic studies that the electronic structure of the WOC remains essentially the same upon the removal of Ca2+ from the WOC.309 On the basis of these results, instead of being an essential structural component, Ca2+ could be important in processes such as PCET between YZ and the Mn4CaOx cluster, and/or it could serve as the initial binding site for substrate water.146,309,310 In this context, as discussed by Yachandra and Yano,146 the changes in the Mn− O−Mn vibrational frequencies,311 the EPR properties of the WOC,302 the rate of water exchange upon substitution of Ca2+ with Sr2+,312 and the results obtained by X-ray spectroscopy all suggest that the critical oxygen atom may be part of a Mn−O− Ca/Sr bridging structure.15 Regarding artificial models for the WOC, Agapie et al.313,314 reported that the insertion of Ca2+ into multinuclear Mn complexes can stabilize high oxidation states of Mn ions. Many studies confirm that Ca2+ ions are important for the stability/ assembly of the WOC system.313 Recent data show that the enthalpies of formation of Mn−Ca oxides from Mn oxides indicate exothermal processes, most probably because of the strongly basic nature of the CaO that combines with the relatively acidic Mn oxides.315 The effect could be important for the stability of the Mn−Ca cluster in PSII. Two Cl− ions are required for water oxidation,316 and Cl− binding sites have been detected in the crystal structure of PSII at atomic resolution.84,85,141 Because the Cl− ions are located at the entrances of two possible proton exit paths, it was suggested that the ions are important in proton transfer.85 In addition to proton transfer, the primary role of Cl− was also proposed to be the stabilization of the configuration of the charged amino acid side chains close to the WOC.137 During the S-state cycle, different conformations, protonation states, and hydrogen bonding of D1Asp61 could support conformational changes of D1-Asp61 with the coupled Cl− as being an essential component of the deprotonation mechanism of the WOC.317 As Cl− and Ca2+ ions are important components in the efficient biological catalyst, the effect of these ions should be more carefully considered in the artificial models.

7.8. The Nanoscale of the Mn−Ca Cluster

An increase in the surface-to-volume ratio results in nanoscalelevel size effects in comparison to the bulk phase.287,288 Thus, redox equilibria and the stability of the transition-metal oxide phase are affected, resulting in differences in the activity of nanoscale metal oxides and their bulk equivalents.289 On the nanoscale, most of the active sites are on the surface, where they can work directly as water-oxidizing sites. The Mn4CaOx cluster in PSII has dimensions of about 0.5 × 0.5 × 0.5 nm3 (Figure 12). Thus, Mn oxides housed in an organic environment may be a good functional model for the Mn4CaOx cluster in PSII.

Figure 12. (A) Mn4CaOx and the amino acids around the cluster. (B) The structure of the Mn4CaOx cluster, depicted as an asymmetric cubane complex that resembles a distorted chair. The image is owned by the Theoretical and Computational Biophysics Group, NIH Resource for Macromolecular Modeling and Bioinformatics, at the Beckman Institute, University of Illinois at Urbana−Champaign.

7.9. Oxidant

The redox potential of YZ/YZ•216,290,291 is around 1.0−1.2 V (vs the standard hydrogen electrode (SHE)), which is high enough to oxidize water. A potential as low as possible should be used in artificial models to prevent decomposition of the catalysts. 7.10. Outer Bonds in the Biological Water Oxidation by PSII

Enzymes usually use the secondary coordination sphere292,293 for the transfer of substrate molecules and protons. The secondary coordination sphere of the WOC is dominated by hydrogen bonding.84,85,110−113,141 The potential required for the wateroxidation process is decreased if the released protons are involved in hydrogen bonds.110−113 Recently, Barry’s group at Georgia Tech suggested that the hydrogen-bonded water ligands may play an important role in the catalytic water-oxidation process.293 Experiments by Polander and Barry293 showed that oxidation of Mn during the S1-to-S2 transition strengthens hydrogen bonding to peptide carbonyl groups. Disruption of this network by ammonia (as a water analogue) decreases the steadystate rate of water oxidation. The results show that the hydrogenbonding network is important in water oxidation. In addition to having a classical hydrophobic protein interior, Dau’s group recently showed that the lumenal side of PSII resembles a complex polyelectrolyte with hydrogen-bonding networks (Figure 13).294 The results show that the hydrogen-bonding network is very important in water oxidation and should be used in design of the artificial models.

7.12. A Four-Electron Water-Oxidation Mechanism

Figure 1 shows that water oxidation is a four-electron reaction or a multistep process involving toxic intermediates, such as •OH, H2O2, or O2−. However, the four-electron water-oxidation process is characterized by the lowest thermodynamic driving force.16 In artificial water-oxidizing catalysts, a four-electron water-oxidation process is also preferred. However, such mechanisms not only use high overpotentials for practical operations, but they also form very active compounds (such as hydrogen peroxide or hydroxyl radicals) that may decompose the catalysts. These harmful compounds are normally well handled in the natural system, and an efficient artificial water-oxidation system must minimize the production of such species during the reaction sequence.

7.11. Roles of Ca2+ and Cl− in PSII

Ca2+ is an essential ion in the WOC because it is required for the water-splitting reaction.149,295−303 Some divalent and trivalent metal ions compete with Ca2+ for the occupation of the Ca2+ site,304−306 but only Sr2+149,307 can functionally substitute Ca2+. It has been proposed that a MnVO moiety is subject to nucleophilic attack by a hydroxide ion linked to a Ca2+ ion,244

7.13. Redox Accumulation in the WOC

The Mn4CaOx cluster is considered a redox accumulator, because it stores four oxidizing equivalents arising from four 2901


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Figure 13. Hydrogen-bonding (HB) networks located the furthest away from the WOC (HBN7−HBN11). The approximate distance to the WOC is indicated in (A) and (B), and in (D) and (E). In (C), the distance between D2-Asn338 and the WOC is ∼33 Å. CP47-Arg357 contributes to both HBN7 (A) and HBN9 (C). Note that D2-Asp297, Glu323, and Glu326 contribute to both HBN10 (D) and HBN11 (E); D2-Thr313 (HBN11, (E)) is also part of HBN2 (not shown; see ref 294). In (B), CP47-Asp433 connects the two halves of HBN8, the CP47-Glu435 side, and the CP47-Gln338 side. Reprinted with permission from ref 294. Copyright 2012 Elsevier.

7.15. Amino Acid Side Chains

individual one-electron reactions (Figure 6). Most probably, in biological water splitting, oxidation of two or three Mn ions occurs to facilitate the four-electron reaction.19 During the catalytic cycle, the WOC is expected to accommodate and accumulate multiple electrons without large structural changes, and each of these properties must also be considered when designing novel water-oxidizing catalysts.

The WOC may be regarded as a Mn4CaOx cluster that is embedded in a protein matrix. Nevertheless, only several amino acid side chains interact with the Mn4CaOx cluster.84,85,141 The roles of most of the residues in the vicinity of the WOC are not known, but at least several of them should affect the charge balance and electrochemical properties of the Mn atoms, assist the coordination of water molecules to the corresponding metal ions, contribute to the well-defined hydrogen-bond network, and improve the overall cluster stability. The PSII PsbO subunit (also referred to as the Mn-stabilizing protein) is a conservative external protein factor; it connects the WOC active site to the lumen and participates in a proton-transfer network.84,85,141,160,218,318−320 The systematic deletion of amino acids from the vicinity of the WOC results in a lower oxygenevolution rate. Moreover, the Mn−Ca cluster deprived of its amino acid environment is less active than the WOC Mn4CaOx complex.321 In the design of artificial models for water oxidation,

7.14. Regulating the Oxidizing Power in Each Charge-Accumulation Step

The Mn4CaOx cluster is modified during the catalytic cycle with the oxidizing power of each S state regulated to inhibit the formation of other intermediates that require higher potentials (•OH, H2O2, and O2−). To achieve similar regulation in artificial models, not only the ability to accommodate and accumulate multiple electrons, but also PCET and optimized structures for each S state need to be considered. 2902


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the amino acid ligands and/or second coordination sphere residues can be replaced by completely different organic or inorganic groups with the goal of providing a more stable environment than that provided by the native polypeptides.

high oxidation state, spin density on an oxygen atom (O•) also helps to increase the acidity (eq 15):

7.16. Binding Sites for Water Molecules

Such insights from Mn or other metal ion chemistry plays an important role in the design of efficient artificial catalysts.

M(H 2O•)n + (aq) → H+(aq) + M−O•H(n − 1) +(aq)

An important role of enzymes is to bind substrates in suitable geometries. As discussed in previous sections, there are many water molecules in the vicinity of the WOC in PSII, but only four water molecules directly coordinate to the Mn4CaOx cluster. Two water molecules coordinate to the Mn ion located outside of the cubane complex, and two water molecules coordinate to the Ca2+ ion.84,85,141 Some of the five bridging oxygen atoms and bulk water molecules in the structure have been considered possible candidates for substrates for the formation of O2.84,85,141,322 With the current available knowledge, either bridging oxygen atoms or water molecules could be substrates for the evolution of O2. A complete understanding of the mechanism of water splitting by PSII will be fundamental to the design and synthesis of efficient artificial catalysts for water oxidation.

7.19. Self-Repair

Catalysts of multielectron processes are likely to change their structure and stability in the course of a turnover.331 This underlines the importance of designing self-repairing catalysts for energy research. As a result of oxidative degradation, the entire D1 polypeptide in PSII is completely replaced every 30 min.332−334 This polypeptide possesses a C-terminal sequence, making it possible to insert pD1, a precursor of the D1 protein, into the thylakoid membrane within the cell.335 This sequence is subsequently cleaved, exposing the C-terminal alanine-344 residue, which acts as a ligand that binds Mn during the photoassembly of the WOC.336 Thus, as a result of a natural process, the Mn4CaOx cluster of the PSII WOC system is degraded and regenerated every 30 min under normal sunlight. Nature therefore uses an efficient self-repair mechanism to solve the problem of instability. Hence, it is intriguing that the recently reported successful water oxidation catalyzed by a synthetic cobalt phosphate heterogeneous catalyst is accompanied by selfrepair of the catalyst;337 the self-repair mechanism was also investigated in other Mn oxides.338,339 Thus, in addition to efficiency, the stability of water-oxidizing compounds is very important. There are at least two ways to improve the stability. The first strategy is to use a very stable catalyst with very high turnover numbers, and the second one is to use a catalyst with self-healing capability.

7.17. Photosystem II as a Photoassembled Complex

The WOC in PSII is formed by a photoassembly process (see section 6.1).323−325 Thus, photoassembly (or self-assembly) could be a strategy for the synthesis of an efficient catalyst. Regarding this issue, an amorphous Ca/Mn oxide phase without any preassembled Mn/Ca precursors, with a structure related to that of the WOC, has been reported.321 This supports the idea that detailed insights into the mechanism of the assembly of the WOC should bring new developments for the design of efficient water-oxidation catalysts. A proposed mechanism for the assembly of the WOC in PSII is shown in Figure 4. 7.18. Chemistry of Mn

7.20. A Different Strategy To Protect from Light

A number of natural enzymes contain Mn2+ and/or Mn3+ ions as cofactors. Mn chemistry is dominated by the occurrence of multiple oxidation states, and many reactions that incorporate disproportionation and comproportionation steps may occur for this ion. The most frequently found oxidation states of Mn in living systems are II, III, and IV. It has been suggested that the oxidation states of the four Mn ions of the WOC are (III, III, III, IV), (III, III, IV, IV), and (III, IV, IV, IV) for the S0, S1, and S2 states, respectively.101 It is known that the oxidation-state changes occurring in the S0 → S1 and S1 → S2 transitions of the WOC are Mn-based. High oxidation states of Mn ions in this compound inhibit the decomposition of the complex and protect it from leaching Mn into solution. Metal-coordinated water ligands have lower pKa326−329 values than free water (as low as 7), when dipositive metal ions are considered. Upon coordination of water to such a dipositive metal ion, the oxygen atom donates two electrons to the metal ion and formally becomes positively charged (eq 14): M(H 2O)n + (aq) → H+(aq) + M−OH(n − 1) +(aq)

(15)

In plants, the rate of PSII repair is usually the same as the rate of decomposition. Nevertheless, under the influence of stress factors or too intense light, this relation might change, so that the rate of damage is higher than the rate of repair. The movements of chloroplasts upon irradiation may form a possible mechanism in plants to minimize photoinhibition of the WOC. For example, chloroplast movements give rise to protection of PSII against intense light by altering the distribution of inhibiting agents in leaves.340,341 Under low levels of irradiation, the internal rearrangement of the chloroplasts results in exposure of PSII to illumination, allowing for a more efficient absorption of light than the light-avoiding arrangement.340,341 On the basis of this study, the chloroplast movements may lead to an increase in the photosynthetic efficiency in leaves in at least two ways: (i) light absorption is affected to maximize photosynthetic output, and (ii) at the same time, it redistributes PSII damage throughout the leaf to reduce the amount of inhibition received by individual chloroplasts, thus preventing a decrease in the photosynthetic capacity.340,341 Such strategies could be used in the design of the artificial photosynthetic systems.

(14)

7.21. Vibrations in Enzyme-Catalyzed Reactions

The pKa of coordinated water ligands in metal complexes is controlled by the coordination number and by the total charge of the complex: the pKa decreases with a decrease in the coordination number and with an increase in the positive charge. MnIII or MnIV ions are present in many complexes with bridging/ terminal oxo ligands, as the pKa of water ligands bonded to highvalent metal ions is considerably lower than that of free water.330 MnIV−OH, MnIVO, and/or MnVO are suggested to be important intermediates in water oxidation.330 In addition to a

Vibrations and their potential involvement in enzyme-catalyzed reactions have been considered in recent years. The importance of vibrations was inferred through computational studies, the consistency of experimental data with contemporary models for catalysis, and through the direct observation of a pressureinduced active-site compression that is consistent with barrier compression.342 Special vibrations in enzymes can reduce the width and height of energy barriers along the reaction coordinate. 2903


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Scheme 1. Comparison of [RuII(bpy)3]2+ (A) and Chlorophyll (B) in Artificial and Natural Water Oxidationa

These vibrations could be important in biological water oxidation and the transfer of protons from the active site.342 Nevertheless, the role of protein dynamics in catalysis requires further investigation, both by experimentalists and by theoreticians.341−343 The role of the group dynamics around active sites in decreasing the activation energy for different reactions has rarely been considered when designing catalysts.

8. ARTIFICIAL MODELS Energy stored in hydrogen can be released by direct combustion, or by fuel cell operations, or by catalytic combustion; hence, hydrogen is a very versatile energy carrier. As described above, a promising way to produce hydrogen is water splitting. However, the water-oxidation reaction is difficult to achieve,10,344 and overpotentials of 400 mV or more are often required to drive water oxidation, which represents an energy loss of 25% in water splitting.9,345 Therefore, finding an efficient water-oxidizing catalyst is of paramount importance for hydrogen production via water splitting.9,345 In recent years, significant attention has been devoted to the development of novel water-oxidizing catalysts that can be used in electrolyzers or as a part of photoelectrochemical devices.346 Rare, expensive, and toxic metal ions, such as platinum and iridium, are typically used for water oxidation in these technologies.347 However, cyanobacteria, algae, and higher plants, by controlling molecular environments and suppressing unfavorable oxidation reactions, manage to use abundant transition metals for the same purpose.141 Therefore, the properties of the WOC provide a blueprint for efficient water oxidation at room temperature.

a

Panel A: After excitation, [Ru(bpy)3]2+ requires a sacrificial oxidant, such as S2O82− or [Co(NH3)5Cl]2+, for the irreversible net conversion of [Ru(bpy)3]2+ into [Ru(bpy)3]3+. In the next step, [Ru(bpy)3]3+ can then act as an oxidant. In panel B, the analogous reactions in oxygenic photosynthesis are shown. Chl (chlorophyll), after excitation to Chl* (singlet excited state), requires CO2 for the irreversible net conversion of Chl into Chl+. In the next step, Chl+ can then act as an oxidant ((CHO)n = carbohydrate). Reprinted with permission from ref 321 with modification. Copyright 2010 John Wiley & Sons, Ltd.

8.1. Oxidants in Water Oxidation

The selection of oxidants is important in the reactions that are included in the water-oxidation process. In these reactions, the catalyst is first oxidized, either chemically (by an oxidant348) or electrochemically, after which the oxidized form of the catalyst oxidizes water to produce oxygen and protons. Several oxidants are used for water oxidation in artificial photosynthetic systems; the performance of these oxidants has been investigated over a range of conditions to determine their efficiency. In this section, we focus on a variety of oxidants that are used (see an excellent review in ref 348 for additional details). 8.1.1. Ru(bpy)33+. The tris(2,2′-bipyridyl)ruthenium(III) cation ([Ru(bpy)3]3+)349 is often used as an oxidant for the water-oxidation process. This cationic complex is formed in the reaction between [Ru(bpy)3]2+ and PbO2 or by photoinduced oxidation of [Ru(bpy)3]2+ with a sacrificial oxidant that is reduced in an irreversible process (Scheme 1).348−350 In this example, the excited sensitizer, [Ru(bpy)3]2+, is oxidized to [Ru(bpy)3]3+ by an electron acceptor; subsequently, [Ru(bpy)3]3+ oxidizes the multielectron-transfer catalyst. In the end, two water molecules are oxidized to form one oxygen molecule on the surface of the catalyst.349 Peroxodisulfate (S2O82−) or [Co(NH3)5Cl]2+ are both irreversible electron acceptors commonly used to photogenerate [Ru(bpy)3]3+ in aqueous media. The reaction of the excited Ru(bpy)32+ by peroxodisulfate to produce Ru(bpy)33+ can also form sulfate radicals as a very strong oxidant (E° ≈ 2.2 V vs Ag/AgCl), which may be the true oxidant in this case.348 A comparison of the reactions involved in O2 evolution from water in the presence of [RuII(bpy)3]2+/[Co(NH3)5Cl]2+ and through photosynthetic water oxidation is shown in Scheme 1.

Experiments showed that, in a solution of [Ru(bpy)3](PF6)3 without a water-oxidizing catalyst, the oxidant decomposed without any detectable production of oxygen, although a small amount of carbon dioxide was produced. The potential of the [Ru(bpy)3]3+/[Ru(bpy)3]2+ redox couple in aqueous solution (E1/2) is 1.23 V vs SHE. 8.1.2. Cerium(IV) Ammonium Nitrate (CAN). CAN is also often used to induce the water-oxidation process. CAN is a commercially available nonoxo-transfer agent that is a oneelectron oxidant. Its solubility and stability in aqueous solution allow it to be used as the primary oxidant in water oxidation catalyzed by Ru and Mn complexes.348,351,352 Three cautionary points should, however, be considered in the use of CAN for water-oxidation experiments. First, CAN is not a simple oxidant: CAN or CeIII (a product of the reduction of CAN) may exchange with the metal ions in the complexes.353 In other words, CAN may not only act as a simple oxidant but also be coordinated by ligands.353 Second, a solution of CAN contains not only mononuclear but also multinuclear species.354 The multinuclear species may transfer two or more electrons at the same time. Hence, CAN may not always act as a one-electron oxidant. Third, many metal complexes react in the presence of CAN under very acidic conditions (pH ≈ 1). These complexes can be decomposed into nanosized metal oxides that are efficient catalysts for water oxidation.355,356 However, the ligand in the metal complex is an important factor in the formation of metal oxides; different ligands can result in different amounts, phases, 2904


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Table 4. Advantages and Disadvantages of Primary Oxidants for the Water-Oxidation Reaction348 oxidant CAN Ru(bpy)33+ S2O82− SO52− IO4− ClO−

advantages

disadvantages

nonoxo, one-electron oxidant; commercially available; trackable by UV−vis spectroscopy nonoxo, one-electron oxidant; trackable by UV−vis spectroscopy stable; commercially available commercially available; stable up to a pH of about 5.0 commercially available; stable at pH 2−7.5; pH remains constant during water oxidation commercially available; may be used in alkaline solutions

stable only at low pH; the ion may replace the metal ion in the complex; the acidic solution may decompose many complexes; strong oxidant that may decompose complexes; NH4+ and NO3− implicated in water oxidation expensive; provides a very small overpotential; only stable in acidic solutions; reduced to Ru(bpy)32+; should be prepared as a fresh solution very powerful oxidant; SO4•− radical produced in the reaction may be involved in water oxidation two-electron oxo transfer two-electron oxo transfer; iodate ion produced during the reaction is a powerful oxidant and may be involved in water oxidation two-electron oxo transfer

the complex with bulky substituents (R = t-Bu) has catalytic activity for water oxidation.360 8.2.1. Mn−Schiff Base Complexes. Several MnIII complexes of the type [{MnL(H2O)}]2+, where L is the dianionic form of an O,N-donating Schiff base ligand, have been shown to induce oxygen evolution and to promote the reduced pbenzoquinone (BQ) upon irradiation with visible light, as illustrated in Figure 14.361,362

or morphologies of metal oxides. As a consequence, different complexes show different water-oxidizing activities.355 It is noteworthy that the standard potential of CAN is 1.70 V vs SHE, which is about 500 mV more than necessary for water oxidation at pH ≈ 0.357 8.1.3. Other Oxidants. Several oxo-transfer compounds, such as H2O2, ClO−, IO4−, t-BuOOH, and SO52−, have also been used as oxo-transfer oxidants.245 In these cases, the observed oxygen-evolution rates may result from oxidants involved in complicated reactions, such as the disproportionation of peroxides when they are used as the oxidants.348 18O-isotope labeling experiments showed either no incorporation of 18O into the evolved oxygen at all (H2O2, BuOOH) or only to an extent of 50% (HSO5−).245 In other words, mechanisms different from that of the water-oxidation reaction may have been involved in these oxo-transfer oxidants. In these examples, the use of oxygentransferring oxidants usually does not result (or only partially results) in water oxidation.348 Therefore, oxygen evolution, rather than water oxidation, is the appropriate description for these reactions. Recently, the research groups of Crabtree and Brudvig introduced IO4− as a primary oxidant for water oxidation.358 Because of the relatively low oxidizing capability of sodium periodate solution relative to solutions of other common primary oxidants, IO4− could only be used as a water-oxidizing catalyst with a low overpotential. The two groups proposed that studying oxygen-evolution catalysis using IO4− as the primary oxidant may provide preliminary information as to whether a catalyst displays a low overpotential for water oxidation.358 Table 4 shows advantages and disadvantages of various oxidants.

Figure 14. (A) Structure of the [Py2NR2Mn(H2O)2]2+ (R = H, Me, or tBu) complexes. (B) The water-oxidation reaction accompanied by the reduction of p-benzoquinone to hydroquinone in the presence of a Mn− Schiff base complex and light.

The active complexes exhibit a band at 590 nm in visible spectroscopy, which is absent for the inactive complexes. The rate of O2 evolution is dependent on the concentration of the MnIII complex (first order), the quinone concentration (order of 0.5), and the pH of the reaction medium, and a maximum for photolysis is observed in the 450−600 nm region.361,362 It is interesting that quinone does not absorb light in this region. In 2011, the group of González-Riopedre published four MnIII complexes with Schiff base ligands, described by the general formula [MnLn(H2O)2]2(ClO4)2·mH2O (n = 1−4; m = 0, 1). The applied H2Ln ligands are 3,5-substituted N,N′-bis(salicylidene)-1,2-diimino-2,2-dimethylethane, where R = OEt, OMe, Br, or Cl.363 Mass spectra recorded for some products showed the presence of a [Mn2L2]+ moiety, which might point to a dimeric complex in solution. In the crystal structure, hydrogen bonds involving ethoxo/phenoxo O atoms and water ligands from a different complex molecule occur; these can be considered μ-aqua bridges. Furthermore, π-stacking interactions involving the aromatic rings were found. The group investigated water oxidation in this system, based on the quantitative assay of oxygen and photocatalytically induced changes in the electronic spectrum of quinone. The redox process BQ/H2BQ was followed spectroscopically in the UV range, and the rate of the process decreased during the measurements. The study of an aqueous solution solely containing BQ showed a steady decrease in the BQ concentration upon photolysis, resulting in a mixture of H2BQ and 2-hydroxy-p-benzoquinone without oxygen evolution. It was also observed that oxygen is not produced in

8.2. Models

In 1974, at the time of the first oil crisis, Calvin proposed the utilization of [(bpy)2MnIII(μ-O)2MnIV(bpy)2]3+ for water splitting and photosynthetic solar energy conversion.359 This model inspired many scientists to develop new models. In sections 8.2.1−8.2.5, we review functional Mn-based models for water oxidation, and in section 8.2.6 we consider the issue of Mn complexes decomposing to Mn oxide, and that in such cases Mn oxide is the true catalyst for water oxidation. Mn oxides as wateroxidizing catalysts are then treated in detail in section 8.2.7. Mononuclear Mn complexes are rarely reported to be wateroxidation catalysts; usually, water-oxidation catalysts are dinuclear or multinuclear Mn complexes. However, the Smith group recently reported catalytic reactivity for the high-spin MnII−pyridinophane complexes [(Py2NR2)Mn(H2O)2]2+ (R = H, Me, t-Bu) for the formation of O2. Complexes with R = H or Me catalytically disproportionate H2O2 in aqueous solution, but 2905


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the absence of BQ, and that the application of 2,5-di-tert-butyl-pbenzoquinone instead of BQ did not generate oxygen, possibly because of a steric requirement.363 González-Riopedre and co-workers363 proposed a mechanism for water oxidation in the system, taking into account the report of Awad and Anderson.364 The group of Awad and Anderson364 suggested that, in aqueous solution, light absorbed at 425 nm results in an n → π* transition, which gives rise to the removal of an H atom from a water ligand in the coordination sphere of the Mn ion. Thus, MnIII is oxidized to MnIV, resulting in strong bonding of the hydroxyl groups, which are thereby polarized to assist their deprotonation.364 The transition state may consist of a Mn complex with bridging O ligands, which quickly decomposes with the formation of oxygen and a dimeric [MnIII2] complex with μ-phenoxo ligands.364 Subsequently, it was reported that the [Mn(salen)H2O](ClO4)2 salt [salenH2 = bis(salicylaldehyde)ethylenediimine] oxidizes water in the presence of CAN.365 The cyclic voltammogram of the complex in water, recorded at a scan rate of 50 mV s−l, showed a peak at 1.46 V (vs SHE) for the oxidation of MnIII to MnIV.365 For the complex incorporated into a Nafion film coated electrode, the anodic wave exhibited a much larger anodic current because of water oxidation catalyzed by the Mn complex, and oxygen gas bubbles were observed at these higher positive potentials.365 It was also shown that the oxidation of the complex in Nafion at an applied potential of 1.54 V (vs SHE) induced an increase in intensity of the band at 370 nm with a simultaneous decrease in intensity of the band at 405 nm. Under these conditions, the compound may transform from the oxidized form into a dimeric or polymeric form.365 Nafion has a perfluorinated backbone, which makes it resistant to the highly oxidizing environment required for water oxidation.365 In the same study, a water-oxidation experiment was performed in the presence of CAN. In this experiment, a saturated aqueous solution of the Mn complex (0.2 mM) was treated with an excess of CAN. An insoluble, brown solid complex was formed in the reaction; subsequently, gas bubbles, identified as oxygen and nitrogen, began to form on the surface of the solid Mn complex. The TON of the complex for O2 evolution was 2.7. CAN was completely consumed during the gas evolution process. In the reaction, large amounts of nitrogen, arising from NH4+ in CAN, were also observed (TON ≈ 10).365 It was reported that [Mn2(μ-O)2Cl(μ-O2CCH3) (bpy)2(H2O)](NO3)2 shows a similar activity.366 It has also been shown that H2O2 can be produced in the reaction of [Mn2(BuSalen)2(O)2]·H2O or [Mn2(BuSaltm)2(O)2]·H2O (BuSalen = N,N′-ethylenebis(4sec-butylsalicylaldimine); BuSaltm = N,N′-trimethylenebis(4sec-butylsalicylaldimine)) with HClO4 in acetone at 0 °C (Figure 15).367 Regarding the catalase activity of the complex, Pecoraro has suggested that if hydrogen peroxide were produced, oxygen would evolve from the solution.368 The compound trans-MnIVL2Cl2 (L = N-alkyl-3-nitrosalicylimide) was reported to be active in water oxidation in acetonitrile/water solutions, as illustrated in Figure 16.369 Chloride ions may stabilize the oxidation state of +IV for Mn.369 O2 evolution, which reached a maximum of 0.27 mol of O2 per mole of complex, was monitored with an oxygen electrode and with a pyrogallol solution.369 Because water oxidation requires four electrons under these conditions, a dinuclear intermediate can be proposed. 18O2 was detected when 18Olabeled water was used, which proved that water is oxidized in this reaction369 (Figure 16). However, it was further suggested

Figure 15. Production of hydrogen peroxide by the addition of HClO4 to solutions of the MnIV−Schiff base dimer, as proposed by Boucher and Coe.367

Figure 16. Crystal structure of a trans-MnIVL2Cl2 complex (L = bidentate Schiff base).

that the intermediate HOCl could be produced in this reaction; under acidic conditions, HOCl forms oxygen in the second step.368,370 8.2.2. [(OH2)(terpy)Mn(μ-O)2Mn(terpy)(OH2)]3+. This complex, introduced in 1999, is one of the most important Mn-based complexes for water oxidation (Figure 17).371,372 The complex was used as an O2-evolving complex in the presence of HSO5− or ClO− by Brudvig and Crabtree and co-workers.373 The group suggested a mechanism for the oxygen evolution process at high oxidant concentrations, where the oxygen product contains minimal 18O originating from 18O-labeled water. At lower concentrations of the oxidant, a significant fraction of the product contains a single oxygen atom originating from labeled water; in some cases, both oxygen atoms of the evolved O2 originate from the labeled water.373 The compound shows wateroxidation activity but has a low TON ( 420 nm), O2 evolution was observed. The TON for the Mn complex of the system was 3.4,339 although this was lower than the TON of 15−17 reported for CAN.376 However, the system is an artificial model for a Mn complex in combination with [Ru(bpy)3]2+, and it can act as a substitute for the WOC/P680 combination that is used for O2 evolution in PSII.377

Recently, water oxidation using a series of [(OH2)(Rterpy)Mn(μ-O)2Mn(R-terpy)(OH2)]3+ complexes with 4′substituted terpy (R-terpy) ligands was reported. It is interesting that the Mn ions in the structures are crystallographically indistinguishable for R = H, MeS, Me, EtO, and BuO, whereas they are significantly different for R = MeO and PrO. Furthermore, the second-order rate constants (k2 (mol−1 s−1)) for these compounds were found to correlate with Em of the (MnIII−MnIV)/(MnIV−MnIV) pair: k2 increased by a factor of 29 as Em increased by 28 mV.378 Kurz and co-workers379−381 extended the system and showed that (i) functional wateroxidation catalysts can also be synthesized by adsorbing Mn complexes other than polypyridyl species, and (ii) MnII complexes deposited on clay are inactive, as active materials all contain MnIII and/or MnIV. TiO 2 nanoparticles with [(OH 2 )(terpy)Mn(μ-O) 2 Mn(terpy)(OH2)]3+ cations attached through direct adsorption or through employment of light-harvesting organic ligands are stable in aqueous solution and in the presence of oxidants.382−384 Studies on three TiO2-based materials differing in crystallinity (P25, which contains 85% anatase; D450, which contains nanoparticles sintered at 450 °C in an anatase matrix; and 2907


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followed by oxygen evolution, resulting in two Mn atoms pivoting outward from the open cube. Thus, the [Mn4O4L6] cubane complex could be both a structural and a functional model for the WOC; however, the WOC has a different molecular structure than Mn4 cubane complexes. Very recently, Zhang et al. successfully synthesized a Mn4CaO4 cluster that resembles the distorted chair structure of the native catalyst, which exhibited typical EPR feactures with a multiline and a g ≥ 4.0 signal upon one-electron oxidation;387 this study is an important advance for developing an artificial water catalyst.387 8.2.4. Mn−Porphyrin Complexes as Water-Oxidizing Catalysts. In 1994, Naruta and co-workers reported dinuclear Mn complexes of dimeric tetraarylporphyrins, linked by a 1,2phenylene bridge, that can oxidize water at potentials greater than 1.20 V vs Ag/Ag+.388,389 The catalyst can also act as an oxidant, reacting with olefins such as cyclooctene to yield epoxides, using stoichiometric amounts of m-chloroperbenzoic acid (m-CPBA).390 The corresponding high-valent MnO complex was proposed to be the active species in water oxidation. In 2004, the same group reported the oxidation of the Mn− porphyrin dimer using m-CPBA as the oxidant, and they reported a spectroscopic investigation of the MnVO product391 (Figure 19).

poorly crystalline D70) show that the adsorption of Mn species on the surface of crystalline TiO2 nanoparticles does not favor the formation of the MnIIIMnIV dimer; MnIV4 assemblies are formed instead. [(OH2)(terpy)Mn(μ-O)2Mn(terpy)(OH2)]3+ P25 induces the evolution of oxygen in the presence of CAN. Photoinduced interfacial electron transfer is observed upon covalent linking of the complex through organic chromophores, resulting in the conversion of MnIIIMnIV into MnIVMnIV. In 2013, Das and co-workers placed [(OH2)(terpy)Mn(μO)2Mn(terpy)(OH2)]3+ in metal−organic frameworks. This was the first example of a Mn-based catalyst performing water oxidation at a high rate (turnover frequency (TOF) (mmol O2/ mol Mn) of ∼11 s−1) with CAN as an oxidant.385 8.2.3. A Mn−Oxo Cube from the Laboratory of Dismukes. A Mn−oxo cube [Mn4O4]n+ in a family of “cubane” complexes (Mn4O4L6; L = diarylphosphinate) was reported to be a model for the WOC in PSII.384 The cubane complex spontaneously assembles in high yield in nonaqueous solutions of MnII and permanganate salts. Oxygen is formed in a high quantum yield of 46−100% by a charge-transfer O−Mn transition that results in the dissociation of a phosphinate ligand.384 In dichloromethane solution, the [Mn4O4L6] cubane complex reacts with hydrogen-donating phenothiazine to produce [Mn4O4L6] and [Mn4O4L6]+ species and to remove two water molecules from the core of the complex. Therefore, two of the corner oxo ligands in the cubane unit can be assumed to undergo replacement with two labile water ligands. The release of oxygen from the Mn4O4 cubane core was corroborated by the detection of 18O2 from [Mn4O4L6]384 (Figure 18). Prior to the work on the Mn−oxo cube family, the butterfly (or double-pivot) mechanism was proposed, consisting of alternating metal and oxo units in a cubane structure.386 In this mechanism, the O−O bond is formed across the face of the cube,

Figure 19. Dimeric tetra arylporphyrins linked by 1,2-phenylene, and the proposed mechanism for O2 evolution catalyzed by the complex. See text for more details. Reprinted with permission from ref 391. Copyright 2004 John Wiley & Sons, Ltd.

It is interesting that O2 evolution involving the MnVO species was observed when a small excess of trifluoromethanesulfonic acid was added to the high-valent Mn complex.391 Naruta and co-workers subsequently proposed that the formation of the O−O bond occurs by the attack of H2O on a MnVO group or by a coupling reaction between the oxo groups of both MnVO units. Subsequently, Nam and colleagues392 reported that the reactions of MnIII−porphyrin complexes with m-CPBA, iodosylarenes, and hydrogen peroxide in organic solvents at room temperature led to the formation of porphyrins containing a MnVO moiety. These products were investigated spectroscopically, employing techniques such as UV−vis, EPR, 1H and 19F NMR, resonance Raman, and XAS. These MnVO porphyrins are diamagnetic low-spin species.

Figure 18. Proposed water-oxidation cycle for Dismukes’ complex. This complex is a Mn−oxo cube [Mn4O4]n+ entity. The observed reduction reactions of the complex to yield O2 are indicated. Reverse arrows show the proposed reoxidation steps that regenerate the cubanes. Reprinted with permission from ref 384. Copyright 2008 John Wiley & Sons, Ltd. 2908


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understand their catalytic efficiency.394 Of these complexes, one containing a long aliphatic chain with a terminal carboxylate group as a distal group was shown to exhibit a higher wateroxidation rate than the other catalysts. In other words, as the authors discussed, this effect did not originate from decreased redox potentials, which would result in more favorable thermodynamics for carrying out the water oxidation.393 It was suggested that the improvement in the catalytic activity may result from the preorientation of the incoming H2O nucleophile and from hydrogen bonding between the distal carboxyl group and a hydroxyl group bonded to the high-valent Mn atom. In 2014, the groups of Åkermark and Siegbahn on the basis of density functional calculations proposed a water-oxidation mechanism for this bioinspired Mn catalyst, where the crucial oxygen evolution proceeds from the formal Mn4(IV,IV,IV,V) state by direct coupling of an Mn(IV)-bound terminal oxyl radical and a di-Mn-bridging oxo group, a mechanism quite similar to the presently leading suggestion for the natural system.395 8.2.6. Nanosized Mn Oxide: A Proposed True Catalyst for Water Oxidation. Using a cubane complex (see Figure 18), an efficient water-oxidizing catalyst was prepared by doping complexes into a Nafion polymer matrix.396 This device was shown to be robust and to function for up to 3 days with only a minor loss in activity.396 Additionally, stacks of these devices, powered by dye-sensitized solar cells, achieved solar-to-hydrogen conversion efficiencies of 1%.396 However, in situ X-ray absorption spectroscopy and transmission electron microscopy (TEM) studies recently demonstrated that, in the Nafion matrix, this cluster dissociates into MnII products, which are then reoxidized to form dispersed nanoparticles of a disordered MnIII/IV oxide phase. As shown by the groups of Spiccia and Casey,338 the cluster structure incorporated in Nafion seems to be different from the cubane structure detected in solution. In fact, the structure resembles those of mononuclear MnII complexes. It was shown that a [Mn4O4(O2PPh2)6] cubanelike complex that is embedded in a Nafion polymer decomposes into MnII products, which are subsequently electrooxidized to a disordered Mn oxide phase. O2 is evolved upon photoreduction of this oxide, and MnII compounds are released. Hocking et al.338 proposed that the catalytic activity of many metal complexes under different conditions could originate from metal oxides that are formed by dissociation of the metal complexes. We suggest that this hypothesis may be correct for many delicate catalysts, but care should be taken with this interpretation for stable catalysts. Recently, Artero and Fontecave397 reviewed and analyzed this issue for oxygen and hydrogen evolution reactions. Their analysis highlighted that under strongly acidic/alkaline and oxidizing conditions for either water oxidation or decomposition of coordinated ligands, metal complexes may transform into metal oxide. In other words, very careful characterization of the reactions is necessary to find the true precatalysts and catalysts. The Spiccia group398 has recently shown that many Mn compounds decompose upon contact with acidic Nafion films to release Mn2+ ions, which are later transformed into Mn oxide nanoparticles as a result of electrooxidation; these nanoparticles catalyze water oxidation.398 The researchers found that the MnOx material generated from coordination complexes is catalytically more active than that formed from MnII. For two precursors, [MnIV(Me3tacn)(OCH3)3]+ and [(Me3tacn)2MnIII2(μ-O)(μ-CH3COO)2]2+ (tacn = 1,4,7-triazacyclononane), the TOFs measured at an overpotential of 350 mV were ∼20

Their stability in the presence of base at room temperature may arise from the binding of a hydroxide ion as an axial ligand. Song et al.392 observed that the Mn−O stretching Raman bands of the MnVO porphyrins are in the range 760−790 cm−1 in organic solvents. However, the rate of oxygen exchange between the MnV−oxo porphyrins and H218O was extremely low.392 In a further development, the reaction of a corrole complex with a slight excess of t-BuOOH in acetonitrile was reported.248 The addition of an aqueous solution containing tetra-nbutylammonium hydroxide started a fast release of oxygen, which was confirmed by mass spectrometry. Thus, the detailed mechanism of O2 evolution could be elucidated.248 In the first step, oxidation of the MnIII−corrole complex to a complex with a MnVO moiety takes place. Secondly, a MnIII hydroperoxo complex might be produced. This compound is postulated to undergo oxidation by an oxidant (possibly a MnV−oxo complex) and to lose a proton, resulting in a MnIV peroxy complex. The compound may disproportionate by losing O atoms or undergo oxidation to a MnV product, which is subject to reductive elimination of O atoms to regenerate the starting complex. The formation of the O−O bond is assumed to occur through a nucleophilic attack of a hydroxide ion on the MnVO moiety.248 8.2.5. A Structural and Functional Dinuclear Model for the WOC. A dinuclear Mn complex that contains imidazole groups in place of the benzylic amine groups present in many previously published Mn complexes has also been reported (Figure 20).393 The complex can catalyze photochemical

Figure 20. Karlsson and co-workers’ model for the WOC in PSII.393 The complex contains imidazole groups in place of benzylic amines present in many previously reported Mn complexes. The complex also contains negatively charged carboxylate groups, which were shown to dramatically reduce the redox potentials of the metal center.393 Reprinted with permission from ref 393. Copyright 2011 John Wiley & Sons, Ltd.

oxidation of water when [Ru(bpy)3]2+ is used as photosensitizer and Na2S2O8 is the electron acceptor. The ligand in the complex contains negatively charged carboxylate groups that dramatically reduce the redox potential of the metal center.393 Because imidazole as well as carboxylate groups act as ligands in the WOC, the complex may be considered a structural and functional model for the WOC.393 The catalytic activity of the complex was investigated by the addition of a 480-fold excess of the single-electron oxidant [Ru(bpy)3](PF6)3 in phosphate buffer (0.1 M, pH 7.2). O2 evolution was observed with an initial TOF of approximately 0.027 s−1, and the TON was approximately 25 after about 1 h. The dinuclear complex is expected to cycle between the initial MnIII2 species and MnV2 over the course of the water-oxidation reaction.393 Recently, Akermark’s group reported a library of these dinuclear MnIIMnIII catalysts with different substituents to 2909


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metal complexes into nanosized particles under catalytic conditions is usually easy, but the detection of such particles is difficult because colloidal solutions often appear homogeneous. Under these conditions, many experiments, using different chemical, microscopic, and kinetic studies, should be used to distinguish homogeneous catalysis from heterogeneous catalysis.401 MacFarlane and Spiccia and co-workers studied the fate of the [(OH 2 )(terpy)Mn(μ-O) 2 Mn(terpy)(OH 2 )] 3+ ions under water-oxidation conditions with XAS and UV/vis spectrophotometry.402 The sample matrix, pH, and the choice of the oxidizing agent have a significant effect on the species formed under the catalytic conditions. They reported that at low pH values (4−6), homogeneous catalysis testing in Oxone implied that [(OH2)(terpy)Mn(μ-O)2Mn(terpy)(OH2)]3+ remains intact, whereas in clay intercalate there is strong evidence that the complex breaks down to a birnessite-like phase, and in homogeneous solutions at higher pH, the results are consistent with the same birnessite-like structure identified in the clay intercalate. The molecular complexes, as a source of manganese instead of simple Mn salts, were found to have the effect of slowing the oxide formation and particle aggregation in solution.355 Two Mn oxides were synthesized by hydrolysis of tetranuclear Mn(III) complexes, [MnIII4O2(PhCOO)9(H2O)]N(n-Bu)4 or [MnIII4O2(PhCOO)7-(PyCOO)2]N(n-Bu)4, in the presence or absence of phosphate ions. The structure of the oxides prepared in the absence of phosphate appeared to be di-μ-oxo bridged Mn ions that formed layers with limited long-range order, consisting of edge-sharing MnO6 octahedra.403 The average manganese oxidation state was +3.5 and showed high oxygen evolution activity in a light-driven system containing [Ru(bpy)3]2+ and S2O82− at pH ≈ 7.403 In contrast, the formed oxides in the presence of phosphate ions contained almost no di-μ-oxo bridged manganese ions, and the phosphate groups were acting as bridges between the Mn ions. The average oxidation state of manganese ions was +3. This type of oxide has much lower water-oxidation activity in the light-driven system. The lower activity in the phosphate containing oxide is related to the absence of protonable di-μ-oxo bridges.403 8.2.7. Mn Oxides. As discussed above, many Mn complexes produce O2 in the presence of an oxo-transfer oxidant,404,405 but only a small number of Mn complexes that catalyze water oxidation have been described. The Mn4CaOx cluster in PSII can be considered a nanosized cluster of Mn oxide in a protein environment.406 Thus, nanosized Mn oxides may be considered models for the Mn4CaOx cluster of the WOC.406 Recently, Scandola and Bonchio reported a tetramanganesesubstituted tungstosilicate [Mn III 3 Mn IV O 3 (CH 3 COO) 3 (SiW9O34)]6− that mimics the WOC S0 state.407 The TOF per Mn in the presence of photochemically produced Ru(bpy)33+ is 0.71 × 10−3 s−1.407 Nanotechnology could also help in the synthesis of more efficient catalysts. A nanosized compound can be defined as comprising particles with sizes from 1 to 100 nm (102−107 atoms) from zero (0D) to three dimensions (3D). Two types of size effects may be distinguished at the nanoscale.288 The first effect is the increased surface-to-volume ratio. The second is related to true size effects, which also involve changes in the local material’s properties. Hence, a nanosized compound may exhibit unique physicochemical properties that are different from those of a bulk compound. It has been shown that nanodispersed oxides of transition metals display substantial shifts in redox equilibria, which are caused by thermodynamic

molecules of O2 per Mn per hour, which is more than 10 times higher than that for MnOx films obtained starting with MnII.398 The TOF was 100 molecules of O2 per nanoparticle with a diameter of 10 nm (each nanoparticle with 100 Mn ions) per second.398 Brudvig and co-workers also reported the immobilization of [MnIV4O5(terpy)4(H2O)2](ClO4)6, [Mn4O6(tacn)4](ClO4)4, and MnO2 in Nafion for the photoelectrooxidation of water.399 Photodecomposition was reported for this system.399 In 2012, nanosized Mn oxides were proposed as catalysts for water oxidation in the reaction of some Mn complexes with CAN.355 In these experiments, some Mn complexes with nitrogen donor ligands and carboxylate ligands were synthesized and, in solution, as a solid, or adsorbed on clay, they were treated with CAN. All of these Mn complexes in solution (10−4−10−5 M), in the presence of CAN, produced CO2, a brown solution, and MnO4−. Experiments showed that the brown solution contained Mn3+ ions.355 When solid Mn complexes were added to the CAN solution (≥0.05 M), the formation of a brown colloidal solution was also observed. Energy-dispersive X-ray spectroscopy (EDX) mapping revealed that the solid was a Mn−Ce nitrate.355 All of these experiments show that ligands in these complexes are decomposed and that MnIII nitrate is formed. MnIII is not a catalyst in the water-oxidation process. Hence, it can be rationalized that Mn complexes do not display high catalytic activities for the water-oxidation process in the presence of CAN.355 The adsorption of [MnIIIMnIVO2(bpy)4](ClO4)3 on clay induced O2 evolution from water in the presence of CAN.400 The complex−clay hybrid was also synthesized and treated with CAN solution (∼0.2 M). After only 10 min, the compound was separated and characterized. The major elements detected on the surface of the compound were Mn and O, and small amounts of C and N were also detected. The Mn 2p3/2 binding energy of the coating was consistent with that of MnOx. All important proposed reactions are shown in Scheme 2.355 Scheme 2. Proposed Mechanism for Water Oxidation Catalyzed by Mn Complexes in the Presence of CANa

a

Reproduced with permission from ref 355. Copyright 2012 Royal Society of Chemistry.

Recently, Najafpour and colleagues, as well as the group of Dau, reconsidered [(OH 2 )(terpy)Mn(μ-O) 2 Mn(terpy)(OH2)]3+ on clay as a water-oxidizing catalyst in the presence of CAN. It was found that under the chosen reaction conditions, the complex underwent transformation into a layered Mn oxide phase, which was the real catalyst for water oxidation.356 As discussed by some research groups,401−403 the decomposition of 2910


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Figure 21. Polyhedral representations of the eight Mn oxides reported herein: (A) β-MnO2, (B) R-MnO2, (C) α-MnO2, (D) δ-MnO2, (E) λ-MnO2, (F) LiMn2O4, (G) Mn2O3, and (H) Mn3O4. The light, dark, and black polyhedra represent MnII tetrahedra, MnIII and MnIV octahedra, and Li+ tetrahedra, respectively. Black spheres represent K+ ions. Reprinted with permission from ref 287. Copyright 2013 American Chemical Society. (I) Combined polyhedral/ball-and-stick representation of [MnIII3MnIVO3(CH3COO)3(SiW9O34)]6−. Reprinted with permission from ref 407. Copyright 2014 John Wiley & Sons, Ltd.

factors.289 Hence, the redox potential assigned to Mn nanoclusters can differ from that assigned to bulk Mn oxides.289 The most important Mn oxides that have been reported to be wateroxidizing compounds will be discussed in this section. There are more than 30 different crystal structures for Mn oxides/hydroxides (see Figure 21 for some Mn oxide structures) in a range of Mn oxidation states. There are many good reviews on the structures and reactivities of Mn oxides,408−411 but here we will focus on the water-oxidizing activity exhibited by Mn oxides. In 1968, Glikman and Shcheglova412 showed that Mn oxides catalyze the oxidation of water to oxygen in the presence of CAN as an oxidant. Subsequently, Shaflrovich and Shilov 413 investigated whether the catalytic properties of MnIV would be preserved when it was incorporated into an organic membrane; they did this by synthesizing Mn oxides bound to a bilayer membrane. Mn oxides in the presence of an oxidant and a bilayer membrane may decompose the organic structure. Shilov and coworkers synthesized their material by ultrasonic dispersion of dipalmitoyl-DL-α-phosphatidylcholine (9.2 mg) in MnSO4 in the presence of borate buffer (pH ≈ 8.3). Gel chromatography coupled with atomic absorption analysis showed that the catalyst contained unilamellar vesicles with strongly bound Mn. The oxidation state of Mn in the compound was estimated to be +III. Upon mixing 5 mL of the catalyst solution with 5 mL of [Ru(bpy)3]3+ solution (10−3 M; pH ≈ 3−4), oxygen evolved. The yield of oxygen per oxidant molecule reached 60−65%.414 The catalytic activity was found to increase upon the

incorporation of the Mn ions in phospholipid membranes. A photocatalytic system was also used with Ru(bpy)32+ as the photosensitizer. In these experiments, Mn ions embedded in the phospholipid were used as the catalyst, and MnIV pyrophosphate was used to accept an electron from the excited Ru(bpy)32+. The oxygen yield was 30%, based on the reduction of the electron acceptor MnIV pyrophosphate.414 Comparing this result with those obtained with other 3d metal ions, Shilov and co-workers showed that the Mn-based catalysts were most efficient for the water-oxidation process in the vesicular system. Furthermore, in contrast to the MnIV clusters, RuO2 catalyzed the oxidation of the lipids instead of water. In the 1970s, Morita et al.415 used MnO2 as an electrocatalyst for water oxidation. They found that a platinum-supported MnO2 electrode showed good anodic characteristics and used a relatively low overpotential for O2 evolution. On the other hand, the use of a titanium-supported electrode as an anode required further modification: despite the good adhesion of the oxide film to the titanium substrate, the high resistivity resulting from the thick film of titanium dioxide needed to be reduced. Morita et al.415 suggested that either the primary water-discharge or the hydroxide-ion-discharge step is rate-controlling in the anodic evolution of oxygen at the platinum-supported MnO2 electrode, both in acidic and in alkaline solutions. They concluded that the MnO2 film is a practical material for the anodic evolution of oxygen as well as chlorine, especially in alkaline solutions. MnIII sites on the oxide surface were suggested to be the active sites for the O2 evolution reaction.416 On the basis of the kinetic 2911


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in PSII. It is therefore interesting that different phases of Mn−Ca oxide showed high efficiencies in water oxidation.422−430 In this regard, a nanosized, amorphous Mn−Ca oxide that had wateroxidation activity in the presence of CAN was synthesized.406 This nanosized, amorphous Mn−Ca oxide potentially bears resemblance to the PSII water-oxidizing complex because it has an analogous elemental composition, similar oxidation states of the Mn ions, and structural and functional similarities.406 The oxide was amorphous, but patterns for a layered Mn oxide were detectable.406 Furthermore, TEM images showed that the oxide consisted of particles less than 10 nm in size. The TOF of the compound in the presence of a 0.45 M solution of CAN was ∼4 times higher than the highest TOF reported for the best Mn oxide catalyst.406 The oxide could be used several times without any significant loss in reactivity. It was again recognized that, because Ca and Mn are cheap and sustainable, this combination seems to be optimal for the design of catalysts for artificial photosynthesis.406,429 Notably, Mn−Ca oxides on the cell walls of the alga Chara corallina431 were also reported to be wateroxidizing catalysts. Various layered Mn oxides with different inert ions (Al3+, Ca2+, Cd2+, K+, Mg2+, and Zn2+) were synthesized, and their wateroxidation activity was compared.339,432 No special effect of the inert ions on the water oxidation was observed; however, these redox-inert ions influence the characteristics of the oxides. For example, Ca−Mn oxides are amorphous until ∼500 °C, but similar compounds containing Cd2+ have a crystalline phase even at ∼300 °C. On the other hand, Kurz and Dau and co-workers prepared a series of K, Ca, Sr, and Mg-containing birnessites. The structural motifs found in these materials showed similar atomic structures despite their different elemental compositions.433 In general, the Ca-birnessites showed the highest activity in water-oxidation catalysis. Water-oxidation rates for Sr-birnessites were lower, but high in comparison to the rates for the Mg-birnessites, which showed only modest activity.433 Interestingly, the wateroxidation experiments indicated that the oxides, like the WOC, require the presence of Ca in their structures to reach a maximum catalytic activity. Thus, water oxidation catalyzed by birnessites displays catalytic trends similar to those found for the native PSII enzyme. However, the effect and the role(s) of the inert ions between the layers of Mn oxides are still an enigma.433 Several key features that are important in determining the efficiency of the layered Mn oxides as catalysts for water oxidation have been recognized; these are315 (i) a layered structure with high thermodynamic stability and a high surface area; (ii) a mixed-valent Mn part with enthalpy values for internal oxidation that are lower than those for the Mn2O3−MnO2 system; and (iii) a low surface enthalpy, indicating relatively weak binding of water to the surface of the nanoparticles. The formation enthalpies assigned to the layered oxides usually point to exothermal processes; this is related to the basic character of these oxides.315 Dau and co-workers proposed that di-μ2-O(H) bridges between the Mn ions lead to a higher number of terminal water coordination sites and increased water-oxidizing activity.434−436 There are many relationships between important factors in water oxidation. These include, for example, the effect of the calcination temperature on the water content, the type of phase and degree of crystallinity, oxidation numbers, and the surface of the material. Hence, for the sake of comparison, all of these factors should be taken into account.432,433

parameters, the group found that the oxidation of the electrode surface of the Mn oxide electrodes is the rate-determining step.415 In 1988, Harriman et al.417 considered metal oxides as catalysts for water oxidation in the presence of CAN or [Ru(bpy)3]3+. They found that Mn, Co, Ir, and Ru are efficient catalysts for water oxidation, and among Mn oxides, MnIII oxide was shown to be an efficient catalyst.417 These researchers also obtained colloidal Mn oxide in the gamma radiolysis of Mn(ClO4)2 aqueous solutions saturated with N2O, displaying a distinct peak at 330 nm.417 Particle diameters were determined using light-scattering studies (6 ± 1 nm) and kinetics (4.2 nm).418 Aggregation processes were observed on standing, and after 3 months this resulted in a material with an average particle size of ca. 70 nm.418 This material displayed a low catalytic activity for water oxidation, with a low yield of only 17.6% of the overall number of oxidizing equivalents and with a low rate of O2 evolution.418 Interestingly, it was reported that MnO2 can act as a diffusion barrier layer for chloride ions. In addition to this, it was shown that the addition of small amounts of Mo, W, and Fe to MnO2 enhanced the oxygen evolution efficiency. For example, a Mn−W mixed oxide exhibited an efficiency of about 99.6% for oxygen evolution,419 while a Mn−Mo oxide showed a 100% oxygen evolution efficiency in the electrolysis (current density of 1000 A m−2; 3.5 wt % NaCl solution; pH 12; and 30 °C).420 In another development, the group of Frei revealed that nanoclusters of Mn oxides combined with mesoporous silica supports are efficient catalysts for water oxidation in aqueous solution under mild conditions.421 This group observed that Mn oxide clusters are exclusively formed inside the silica host and that they do not disrupt the cubic mesopore structure. The mean diameters of the Mn oxide clusters were 73−86 nm. Mn K-edge XAS showed that materials calcined at 500, 600, and 900 °C mainly contain MnIV, MnIII, and MnII,III, respectively. It was confirmed that the nanoclusters of Mn oxides captured inside of the silica phase display good water-oxidizing activities at room temperature and mild pH, with a low overpotential of 350 mV (E°([Ru(bpy)3]+3/[Ru(bpy)3]+2) = 1.23 V vs SHE; E°(O2/ H2O) = 0.89 V vs SHE at pH 5.6).421 They also found that Mn2O3 calcined at 600 °C is the most efficient catalyst for water oxidation. They obtained TOFs of 1630, 1210, 3330, 1260, 1590, and 1830 s−1 per Mn oxide nanocluster for Mn oxide on mesoporous silica that was calcined at 400, 500, 600, 700, 800, and 900 °C, respectively. The oxygen yield using an aqueous suspension of micrometer-sized Mn2O3 was 26 times lower than that obtained when the bulk material was used. They proposed that the high-surface-area silica support may be critical for the integrity of the catalytic system by offering a perfect and stable dispersion of the nanostructured Mn oxide clusters. 421 Interestingly, it was proposed that the silica surroundings could influence the stability of the Mn oxides by protecting the catalytically active Mn centers, which might be deactivated by surface restructuring. This environment could also enhance photocatalytic deprotonation, thereby avoiding acidic conditions and limiting leaching of the Mn catalyst.421 In studies aiming to simulate the Mn4CaOx cluster in PSII, it was shown that the incorporation of Ca ions into Mn oxides improved the catalytic activity of these synthetic oxides.321 However, as shown in Figure 12, the Mn4CaOx cluster in PSII has dimensions of about 0.5 nm;84,85,141 hence, nanosized or, more interestingly, angström-scale Mn or Mn−Ca oxides may be better structural and functional models for the Mn4CaOx cluster 2912


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Figure 22. (A) Schematic image of zeolite Y. Exchangeable sites are found in site I. Site II is displaced from this point into a supercage. Sites I′ and II′ lie in the sodalite cavity, on the opposite sides of the corresponding six-rings of sites I and II, respectively. Site III lies opposite to a four-ring inside the supercage and site III′ of site III. (B) TEM image of nanoscale Mn oxide within a faujasite zeolite sample, with a Mn content of 1.0 wt %. The dark area shows the Mn oxide. Considering the size (1.3 nm) of the supercage of faujasite zeolites and the formation of a small portion of mesopores after the 2913


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Figure 22. continued precipitation of the Mn oxide, it is concluded that most of the Mn oxide particles are located inside the supercages. (C) TEM images of the MnIII,IV oxide monosheets. (D) Schematic representation of the structure of the self-assembled layered hybrid [Ru(bpy)3]2+ between the layered Mn oxides (cyan spheres denote water molecules). (E) Photograph of the soluble form of Mn oxide. (F) SEM micrographs of particles in the soluble Mn oxide after the aggregation of colloidal particles. Copyright 2012 Royal Society of Chemistry. (G) The crystal structure of Li2MnP2O7. The inset shows the local environment around the Mn2O9 subunit (blue). The pyrophosphate units and the Li atoms are depicted in gray and green, respectively. Reprinted with permission from ref 454. Copyright 2014 American Chemical Society.

Recently, Zhou et al.437 reported that the thermal treatment of MnOx films (obtained from aqueous solutions) at 120 °C for 30 min induced their conversion into films with high catalytic activities. In this study, XAS results demonstrated the growth of small amounts (3−10%) of reduced Mn species (MnII or MnIII) after heat treatment. Zhou et al.437 concluded that the thermal treatment is mainly a dehydration process that results in the permanent loss of structural water and hydroxyl groups; however, reduced Mn species are also important. Nanoscale Mn oxides within faujasite zeolite were also reported to be efficient catalysts for water oxidation.438 TEM images of a sample with a Mn content of 1.0 wt % were reported. These indicated the presence of particles 0.7−2 nm in size (a maximum in the size distribution was found at 1.3−1.5 nm).438 Mn oxides combined with faujasite zeolite are among the best Mn-based catalysts for water oxidation in the presence of CAN, with TOFs of ∼2.6 × 10−3 s−1 (Figure 22A and B).438 Recently, the water-oxidizing activity of amorphous Mn oxide coated montmorillonite hybrids was also reported.439 The compounds were synthesized by the reaction of MnII (adsorbed on clay) with MnO4− in the presence of NaOH. EDX mapping images showed piles of Mn oxide on clay. The compounds showed good water-oxidizing activities (TOF = 2.1 × 10−4 s−1) with TONs of ∼3 after 1 h in the presence of CAN. Nevertheless, as this material was heated to 700 °C, the formation of a buserite (Na4Mn14O27·21H2O) phase was detected; the structure of buserite is related to that of birnessite, but differs by the presence of a double H2O layer.439 As compared to many other Mn oxides, the material exhibits increased leaching of the Mn ions. Thus, the stability of layered Mn oxides formed on a clay support is decreased.439 As discussed in the previous sections, [Ru(bpy)3]2+ is an interesting sensitizer for water oxidation. Many research groups use it as a photosensitizer with [Co(NH3)5Cl]2+ or S2O82− ions as electron acceptors under irradiation with visible light (λ > 400 nm), with the aim of studying a model for PSII water oxidation.440 A new strategy, using monosheets, to arrange [Ru(bpy)3]2+ (photosensitizer) with MnIII/IV oxide (wateroxidizing catalyst) into a self-assembled, layered, hybrid [Ru(bpy)3]2+/Mn oxide, was also reported.441 To produce the compound, the Mn oxide monosheets (Figure 22C) were synthesized using a very simple method: the reaction of MnCl2 with H2O2 in the presence of tetramethylammonium hydroxide.442 In the presence of [Ru(bpy)3]2+, the MnIII,IV oxide monosheets aggregated to form layered structures (Figure 22D).441 This strategy may increase the rate and yield of the water-oxidation process, as the interactions between the [Ru(bpy)3]2+ ions are reduced. A rate of O2 evolution of 7.0 μmol of O2 (mol Mn)−1 s−1 was detected in the absence of [Ru(bpy)3]2+ cations, using a 250 W tungsten−mercury lamp and [Co(NH3)5Cl]2+ (10.0 mM) as a sacrificial electron acceptor.441 Interestingly, when salts were added to a mixture of the compound in water, the concentration of [Ru(bpy)3]2+ in

solution increased. The effect was tested for [Co(NH3)5Cl]2+, Al3+, Ba2+, and Cd2+ ions. The decrease in the concentration of [Ru(bpy)3]2+ was observed because of a decomposition reaction (eq 16):441 Ru(bpy)32 + (between layers) + An +(aq) ↔ An +(between layers) + n/2Ru(bpy)32 + (aq)

(16) 2+

In other words, the low concentration of [Ru(bpy)3] in solution may be regulated by applying this strategy. A low and constant concentration of [Ru(bpy)3]2+ cations is very important for increasing the rate of O2 evolution and for decreasing the rate of decomposition of [Ru(bpy)3]3+ because [Ru(bpy)3]3+ can decompose by the reaction between two [Ru(bpy)3]3+ ions or by the reaction of [Ru(bpy)3]3+ with excited [Ru(bpy)3]2+.441 An increase in the photosynthesizer concentration was observed with an increase in the oxidation state of Mn ions. Addition of the oxidant, hydrogen peroxide (without additional ions), to a suspension of the compound in water increased the concentration of [Ru(bpy)3]2+ in solution (eq 17; ε denotes the number of moles of oxidized Mn ions in the presence of the oxidant):441 (Ru(bpy)32 + )a Mn IIIbMn IV cO2 → 2εe− + ε Ru(bpy)32 + + (Ru(bpy)32 + )a − ε Mn IIIb − 2εMn IV c + 2εO2

(17)

The mechanism of O2 evolution by the compound was not reported, but it was suggested that this strategy led to combining the catalyst for water oxidation with the photosynthesizer in one material, to enhance the electron-transfer catalyst and photosynthesizer and to keep a constant low concentration of [Ru(bpy)3]2+ cations. Additionally, because the photosynthesizer is a cationic complex and the catalyst is anionic, the electron transfer between them is expected to be faster than electron transfer from the water-oxidizing catalyst to the oxidized sensitizer ([Ru(bpy)3]3+).443 A nanostructured MnIII oxide with both oxygen-reducing and water-oxidizing activity was reported.444 The bifunctional, nonprecious Mn oxide thin film was more active for the oxygen-reducing system than Ru and Ir nanoparticles, with only a ca. 130 mV difference in activity with respect to the Pt half-wave potential. Mn oxides in the form of a thin film were more active than Pt, with rates similar to those of Ru and Ir.444 This study related the excellent catalytic activity of the nanostructured compound to the proper MnxOy active sites at the relevant potentials to drive both the oxygen-reducing and the wateroxidizing activities.444 Nanosized λ-MnO2 was prepared by the reaction of Mn(OAc)2 with LiNO3 at 350 °C in the presence of urea and citrate in acidic solution to aid the formation of a high-surfacearea material during degassing to remove H2O, NH3, and CO2. The nanosized λ-MnO2 was introduced as an efficient wateroxidizing catalyst in the photochemical Ru(bpy)3]3+/S2O82− system at pH 5.8.445 This study showed that delithiation of nanocrystalline spinel LiMn2O4 by treatment with dilute HNO3 2914


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solution produced nanosized λ-MnO2 (20−100 nm). In fact, the experiments indirectly introduced cubane Mn4O4 units into λMnO2, similar to the Mn4CaOx cluster of the WOC.445 In a different study, a colloidal MnIV oxide phase was prepared through a simple reaction between MnO4− and S2O32−, as illustrated in Figure 22E,F.446 This phase contained spherical particles with a mean radius of ca. 50 nm, stabilized in solution by the presence of electrical charges. Recent studies show that the colloidal MnIV oxides are catalysts for water oxidation in the presence of Oxone, H2O2, CAN, and [Ru(bpy)3]3+.447 It was shown that under the reported conditions, the activity of the material substantially exceeds the activities of bulk MnO2 and αMn2O3. Decisive factors affecting the high water-oxidizing activity of this colloidal MnO2 phase may include the small particle size, their dispersion, and charge.447 α-MnO2 is a polymorph containing the largest 2 × 2 channels, which are formed by edge-sharing of octahedral MnO6 units. Therefore, this phase readily adsorbs guest cations. Jiao’s group studied the water-oxidizing activity of α-MnO2 nanotubes, αMnO2 nanowires, and β-MnO2 nanowires.448 SEM images displayed that the pristine α-MnO 2 nanotubes are of homogeneous morphology, with outer diameters of 100 ± 30 nm, inner diameters of 40 ± 20 nm, and lengths of 0.5−3 mm. The SEM images of β-MnO2 revealed nanowire morphology, with a typical length of 2 ± 1 mm and a diameter of 30 ± 20 nm. On the basis of EDX results, the pristine α-MnO2 nanotubes and nanowires contain ca. 10.5 atom % of K+, whereas bulk α/βMnO2 nanowires do not contain potassium.28,44 α-MnO2 nanotubes/nanowires and β-MnO2 nanowires were shown to be crystalline by high-resolution transmission electron microscopy (HRTEM) studies.448 In the [Ru(bpy)3]2+/S2O82− system, by comparing nanostructured α-MnO2 and β-MnO2 polymorphs with other modifications of MnO2 recently reported as catalysts for water oxidation, it has been demonstrated that the crystal structure of these catalysts has a negligible effect on the water-oxidizing activity.448 A TOF of 3.5 × 10−5 s−1 was determined for α-MnO2 nanotubes; TOFs for α-MnO2 nanowires, bulk α-MnO2, and βMnO2 nanowires were determined to be 5.9 × 10−5, 1 × 10−5, and 2 × 10−5 s−1, respectively. It is interesting to note that the TOF values per surface area of these Mn oxides are similar, even for different morphologies (nanotubes and nanowires) and crystal structures (α-MnO2/β-MnO2). It was reported that Mn ions on the surface of the catalyst phase in all three oxides show similar activities for water oxidation. Moreover, independent of their morphologies and crystal structures, most of the MnO2 phases show similar TOF values per surface area. Thus, the morphology and internal structure seem to negligibly influence the activity of the MnO2 catalysts for water oxidation, but the surface area is an important factor in the activity of these compounds.448 It was found that β-MnO2 is inactive in water oxidation. However, Spiccia’s group reported a highly active screen-printed β-MnO2 phase electrocatalyst for water oxidation. The catalyst was prepared by mixing a solution of ethyl cellulose binder with terpineol. At pH 13.6, the catalyst shows current densities of 10 mA cm−2 at η = 500 mV.449 However, it is possible that organic compounds used in the procedure reduce MnIV ions on the surface of the catalyst. Very recently, Suib’s group reported the catalytic activities of α-MnO2, β-MnO2, δ-MnO2, and amorphous MnO2 both for water oxidation and for oxygen reduction under electrochemical conditions.450 Similar structure−activity relationships in alkaline media were observed (α-MnO2 > AMO > β-

MnO2 > δ-MnO2) in both reactions.450 α-MnO2 is stable and needs an overpotential of 490 mV (as compared to 380 mV required by an Ir/C catalyst) to reach a current density of 10 mA cm−2.450 α-MnO2 is also an efficient oxygen-reducing catalyst with a current density of 3 mA cm−2, showing an overpotential of 760 mV, which is close to the overpotential of 860 mV for 20% Pt/C.450 This efficiency was related to the O2-adsorption capability of α-MnO2.450 Recently, Nocera’s group studied water electrooxidation using MnOx films under acidic, neutral, and alkaline conditions. The group reported that under acidic conditions, the initial chemical turnover-limiting step can be assigned to MnIII disproportionation on the surface; under alkaline conditions, a one-electron/ one-proton equilibrium is the limiting step in water oxidation.451 At neutral pH, there is competition between these two mechanisms for limiting the water-oxidation rate.451 It was reported that electrodeposited Mn oxides are more stable than Ni and Co oxides under water-oxidation conditions.451 A few groups studied the effect of anions on Mn oxides toward water oxidation.452 Tak reported that fluoride anions effectively reduce the overpotential required for water oxidation. In accordance with electrochemical studies and XPS results, the group proposed that adsorption of fluoride inside the double layer changes the oxidation state from MnIV to MnIII, resulting in an increase in catalytic activity for water oxidation. Tak et al. reported that a 1 M KOH solution containing fluoride (8 mM) has an exchange-current density that is 1.6 times higher than that of pure 1 M KOH.446 Zaharieva and Thapper prepared Mn oxides by hydrolysis of tetranuclear MnIII complexes in the presence and absence of phosphate ions.453 They reported that the structure of the oxides prepared in the absence of phosphate ions is dominated by di-μ-oxo-bridged Mn ions that form layers with limited long-range order, consisting of edge-sharing MnO6 octahedra with an average Mn oxidation state of +3.5. The oxides are active in water oxidation. However, the oxides formed by hydrolysis in the presence of phosphate ions contain almost no di-μ-oxo-bridged Mn ions, but they contain phosphate groups as bridges between Mn ions. In the compound, which is not a good catalyst for water oxidation, the average oxidation state of Mn is +3.0.453 Regarding these and other Mn oxides, Zaharieva and Thapper concluded that five important factors in water oxidation by Mn oxides are their amorphous structures, the presence of both MnIII and MnIV ions in the structure, a large extent of di-μoxo bridging, the presence of water molecules, and the presence of many defects in the structure.453 In 2014, Kang and Tae reported pyrophosphate-based, crystalline Li2MnP2O7 (Figure 22G).454 An interesting feature of Li2MnP2O7 is that the oxidation state for Mn in this compound can be accurately changed from 2 to 3 by controlled delithiation, which is accompanied by minimal structural changes. There are two different Mn sites in this compound: a trigonal bipyramidal (MnO5) and an octahedral (MnO6) Mn site.454 Li2−xMnP2O7 shows catalytic stability at potentials as high as 1.5 V vs NHE, without delithiation or phase transformation.454 It was also reported that higher MnIII contents result in increased wateroxidation activity.454 Dutta and Suib reported amorphous birnessite-type and cryptomelane-type tunnel Mn oxides as efficient water-oxidizing catalysts (Figure 23).455 The amorphous Mn oxide oxidizes water with a TOF of 5.4 × 10−4 s−1 and a TON of 0.29 mol O2 per mole of Mn after 1 h. Moreover, no phase conversion after reaction with CAN was observed for the catalyst.455 These researchers related the high catalytic activity of the compound to 2915


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plasma and plays an important role in the transport and deposition of both endogenous and exogenous substances. It also interacts with many inorganic species, targeting specific binding sites.457−459 TEM images show very small particles of nanosized Mn oxide attached to the BSA protein. In the complex, the Mn oxide phase is amorphous and was identified with XRD. It was shown that BSA initiates the nucleation process and that it may also prevent the further expansion of the Mn oxide phase; without BSA, larger particles are formed.456 Moreover, the dispersion of Mn oxide in water is unique.456 Using [Ru(bpy)3]2+/K2S2O8 and irradiation with visible light (λ > 400 nm; intensity of 10 000 lx), O2 evolution was observed upon addition of the Mn oxide−BSA compound to an aqueous solution containing tris(2,2′-bipyridyl)ruthenium(II) chloride and K2S2O8.456 The rate of O2 evolution by this compound under these conditions was 140 μmol of O2 (mol Mn)−1 s−1. The nanosized Mn oxide−BSA hybrid is also a good catalyst for water oxidation in the presence of CAN.456 The TOF for O2 evolution by this compound in the presence of CAN (0.1 M) is 2.7 × 10−4 s−1. However, under these conditions, CAN (or [Ru(bpy)3]3+) is a very powerful oxidant that can oxidize and decompose amino acids present in BSA.456 Recently, it was shown that the stabilization of Mn3+ ions on the surface of Mn oxides is an efficient approach for decreasing the overpotential required in the water-oxidation process catalyzed by manganese(IV) oxide.460 The use of poly(allylamine hydrochloride) as a ligand coordinated to the surface Mn ions of MnO2 electrodes helped to stabilize the Mn3+ ions. This resulted in a shift in the negative direction of ca. 500 mV in the water-oxidation onset potential at neutral pH. This value is as low as that measured for the natural PSII system. Recently, soft X-ray absorption and resonant inelastic X-ray scattering at the Mn L-edge were used for studying the electronic structure of Mn oxides in water oxidation.461 Both techniques showed that the most active Mn oxides contain more MnIII than MnII or MnIV.461 In addition to these results, it was found that MnIII ions have the lowest local HOMO−LUMO gap and the most intense charge-transfer emission band.461 In the next step, to find important factors that influence the efficiency of Mn oxides in water oxidation, Spiccia et al. found, through the use of HRTEM and electron-scattering simulations, that sodium birnessite in Nafion exhibits an exceptionally high degree of layer misregistration and a high concentration of Mn vacancies, relative to other Mn oxides.462 Such a structure was also observed in decomposition products of Mn complexes in the presence of other oxidants.463 Recently, Dau’s group reported the switching between the electrodeposition of inactive Mn oxides (at constant anodic potentials) and the synthesis of the active Mn-based catalyst (by voltage-cycling protocols).464 In the active catalyst, separate redox transitions are not readily resolved, which can possibly be explained by extreme broadening of these redox transitions by electronic interactions between the Mn sites in the amorphous compounds. The TOF at 1.35 V (vs SHE) and at room temperature was reported to be around 0.01 s−1 per deposited Mn ion, and molecular oxygen was evolved. On the other hand, on the basis of a calibration employing simple Mn oxides, the average oxidation state of Mn in the active catalyst was estimated to be +3.8, while it was +4.0 in the inactive catalyst. More interestingly, the shape of the XANES spectrum of the inactive catalyst indicated a regular birnessite structure, whereas the shoulders in the XANES spectrum of the active oxide pointed to a more heterogeneous environment. The research group

Figure 23. TEM images (top row): (A) mixed-valent, porous, amorphous Mn oxides; (B) cryptomelane-type tunnel Mn oxides; and (C) layered Mn oxides. HRTEM images (bottom row): (D) mixedvalent, porous, amorphous Mn oxides; (E) cryptomelane-type tunnel Mn oxides; and (F) layered Mn oxides. Reprinted with permission from ref 455. Copyright 2012 American Chemical Society.

its structure, which is layered and analogous to the hexagonal birnessite, having cation vacancies in the MnO2 sheet.455 Cation vacancies in the catalyst are also proposed to be important factors that affect the catalytic activity because of coordinatively unsaturated oxygen atoms, which are excellent sites for proton binding.422,423 All Mn oxides have been reported to be free of amino acid residues with stabilization of the Mn oxide phase, proton transfer, and/or lower activation energy for water oxidation in comparison with the PSII system. Recently, a nanosized (Mn oxide)−(bovine serum albumin (BSA)) hybrid has been shown to be a structural and functional model for the PSII WOC site, as illustrated in Figure 24.456 The BSA protein is soluble in blood

Figure 24. HRTEM image of Mn oxide−BSA. In the case of the crystalline section shown by the red arrow, a layered Mn oxide with the distance of 8−9 Å between layers was observed (yellow lines and blue arrows). 2916


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considered the pH dependence of the anode potential to reach a current level and determined a slope of ∼60 mV per pH unit, which is explainable by formation of an intermediate state by Mn oxidation coupled to the release of one proton. This oxidation and deprotonation step is completed before onset of a relatively slow chemical step, the latter being largely insensitive to both the anode voltage and the buffer pH.464 Related to the above, recent ab initio calculations combined with X-ray spectroscopy showed the localization and structural connection of Mn(II), Mn(III), and Mn(IV) ions in amorphous Mn oxides and the distribution of protons at the Mn oxide/water interface.465 The calculations resulted in models of the Mn oxide atomic structure, formed by the interconnection of Mn-oxo sheets cross-linked through different kinds of defective Mn atoms, arranged in closed cubane-like units.465 Essential for the catalytic activity is the presence of undercoordinated Mn(III)O5 units located at the boundary of the amorphous network, where they are ready to act as hole traps that trigger the oxidation of neighboring water molecules when the catalyst is exposed to an external positive potential.465 As discussed by Wiechen et al., the oxido bridges present at the surface of Mn oxide could be considered as “surface base” and involved in proton abstraction from the substrate water molecules.433 Highly active MnOx/glassy carbon catalysts for water oxidation and oxygen reduction were prepared by atomic layer deposition.466 Atomic layer deposition is a vacuum deposition method that consists of a series of reactions that deposit up to one monolayer of atoms at a time and that can be used to deposit many types of materials, from oxides to metals. Initially, MnO was prepared, but it showed poor activity for the oxygen reduction reaction, although it was an excellent catalyst for water oxidation. However, it was possible to use an annealed MnO film to synthesize Mn2O3 to obtain an efficient catalyst for both the oxygen reduction and the water-oxidation reactions. Thus, atomic layer deposition produces active MnOx catalysts that can be deposited as conformal thin-film coatings over highly anisotropic high-surface-area structures.466 In related experiments, researchers electrodeposited MnOx on fluorine tin oxide (FTO) glass substrate at a high temperature (120 °C), using ethylammonium nitrate as an ionic liquid electrolyte.467 Using a variety of analytical techniques, it was shown that the valence state of Mn in the deposited films can be controlled by changing the electrolyte composition. Along with different phase compositions, a number of different morphologies, including nanowires, nanoparticles, nanofibers, and highly open and dense structures, were obtained by varying the acidity of the electrolyte.467 The film composed of Mn3O4 showed low catalytic activities, whereas birnessite-like Mn oxide and Mn2O3 phases exhibited high catalytic activities for water oxidation.467 In fact, the catalytic activities were also affected by the surface morphology and surface area.467 Their results also indicated that the proportion of Mn in MnOx films decreases when the electrolytes become more acidic; this could imply an increase in the valence state of Mn.467 Mette et al.468 reported on water oxidation catalyzed by nanostructured Mn oxide supported on carbon nanotubes (CNTs). The group functionalized the CNTs using an oxidative treatment to create anchoring groups for the metal precursor. CNTs were either impregnated using an aqueous MnII nitrate solution or used for deposition through precipitation by a comproportionation reaction (eq 18):

3Mn 2 +(aq) + 2MnO4 −(aq) + 2H 2O(l) → 5MnO2 (s) + 4H+(aq)

(18)

The oxidation state is higher for the comproportionated MnOx than for the impregnated sample. The 5 wt % MnO/CNT sample obtained by impregnation showed good catalytic activity for water oxidation at neutral pH, and it was found to display good stability.468 This group also proposed that the compound may be used in combination with efficient photoactive semiconductors, such as d0 and d10 transition metal oxides or oxynitrides. Such carbon/Mn oxide composites are also promising materials for other applications.469−471 Recently, the groups of Dismukes and Greenblatt synthesized pure Mn oxides by adapting literature synthetic methods,287 (Figure 25) and they studied the water-oxidation reaction

Figure 25. HRTEM images of three pure Mn oxides: (A) Mn3O4, (B) Mn2O3, and (C) λ-MnO2. Reprinted with permission from ref 287. Copyright 2013 American Chemical Society.

catalyzed by these oxides. These scientists revealed that the catalytic activities, normalized with respect to the surface areas of the catalysts obtained from Brunauer−Emmett−Teller analyses, follow the order Mn2O3 > Mn3O4 ≫ λ-MnO2.287 They proposed that the electronically degenerate Mn III , having an e g 1 configuration and displaying the Jahn−Teller effect, contributes to the structural flexibility for catalytic turnover in water oxidation at the surface. In addition to these results, it was shown that crystalline Mn oxides exhibit little activity for water oxidation.287 However, complicated relationships between these factors exist in water oxidation. For example, the calcination temperature affects the water content, oxidation number, phase, crystallinity, and surface area. Thus, to compare water-oxidizing activities of Mn oxides, all factors should be carefully analyzed for different phases. On the other hand, the pure phases convert into other phases, most probably layered Mn oxides.472,473 In other words, the purity of Mn oxides (on the surface, at least) may not be high with regard to the phase conversion. The results for water oxidation catalyzed by Mn compounds are collected in Table 5. The mechanism of water oxidation catalyzed by Mn oxides is not known in detail, but there are some proposed mechanisms for this reaction (Scheme 3A).381 Many years ago, it was found that the water-oxidizing activity of Mn oxides significantly increases in basic solution. Recently, Takashima et al.474 2917


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Table 5. Rates of Water Oxidation by Various Manganese Oxide Catalystsc

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Table 5. continued

a

(mmol O2/mol Mn·s). bMany groups reported Mn oxides in electrowater oxidation, but only the best numbers are reported. cImages are reprinted with permission from ref 247. Copyright 2014 American Chemical Society.

layered Mn oxides. Membrane-inlet mass spectrometry (MIMS) was used to detect the oxygen produced in the Mn-catalyzed reactions, and signals for the O2 isotopologues (16O)2 (m/z 32), 16 18 O O (m/z 34), and (18O)2 (m/z 36) were measured.475 The levels of (16O)2, 16O18O, and (18O)2 species quickly rose after the addition of CAN, and (18O)2 was detected. The theoretically expected 18O fraction was reached within only 30 s after the addition of CAN to the oxide suspension. These results confirmed that the oxygen formed in the reactions with CAN

proposed that the decreased water-oxidizing activity under neutral or acidic conditions is due to the instability of MnIII at pH < 9 (Scheme 3B). The presence of MnIII was known to be an important factor for water oxidation.415,416 In other words, at pH < 9, MnIII is unstable and disproportionates to produce MnII and MnIV. At higher pH (>9), the MnIII state is stable enough to participate in water oxidation. In 2011, Messinger and Kurz investigated the oxidation of water with CAN or [RuIII(bpy)3]3+ in H218O, catalyzed by 2919


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Scheme 3. (A) Mechanisms Proposed for the Oxygen Evolution Reaction Catalyzed by Mn Oxides; and (B) Current Density (j) versus Potential (U) Curve for a δ-MnO2 Electrode under Neutral pH Conditionsa

a

(A) (i) Nucleophilic attack of OH2 on a terminal OH, (ii) coupling of terminal OH groups, (iii) attack of OH on a bridging oxido ligand, and (iv) coupling of bridging oxido ligands. Reproduced with permission from ref 479. Copyright 2013 Royal Society of Chemistry. (B) The MnIII species on the surface of the oxide are rapidly consumed by charge disproportionation to form MnII and MnIV, resulting in no net charges passing across the electrode. Reproduced with permission from ref 474. Copyright 2012 American Chemical Society.

or [RuIII(bpy)3]3+ originates from the oxidation of bulk water. From these experiments, it was concluded that (i) the bridging oxido ligands on the surface are not directly involved in the O−O bond formation process ((i) and (ii) in Scheme 3A) and (ii) the bridging oxido ligands on the surface are oxidized to form O2 ((iii) and (iv) in Scheme 3A), but under these conditions, μ-O groups on the surface should exchange with the bulk solution very rapidly. If the exchange is slow, more (16O)2 and 16O18O will be formed, because μ-O groups are not isotopically labeled when O2 is evolved. On the other hand, data reported by many groups indicate that the rates for water exchange with μ-O groups in various Mn complexes are low.476−478 Recently, it was published that μ-O groups on the surface of Mn oxides exchange very slowly with water.479 Regarding the low rates of the μ-O exchange and the MIMS results, the O−O bond may be formed by the attack of an outer-sphere water molecule on an OH group attached to a highvalent Mn ion in the oxide structure or by the reaction between two OH groups coordinated to high-valent Mn ion(s) ((i) or (ii) in Scheme 3A). On the basis of recent theoretical calculations on the mechanism of water oxidation catalyzed by transition metal oxides, similar water-oxidation mechanisms were proposed. A careful analysis shows two types of water-oxidation reactions catalyzed by Mn oxides. One is with low overpotentials (0.030− 0.1 V), related to pathway ii (Scheme 3A);480−482 the other is with higher overpotentials (∼0.5 V), related to pathway i (Scheme 3B).483 Such mechanisms were suggested for Ru oxides.484 Dau et al.436 proposed that the atomic structure is an important factor for water oxidation catalyzed by Mn oxide. The group suggested that the presence of di-μ-oxo-bridged Mn ions in the layered structure is coupled to redox and charge-capacity behavior. The layered structures ensured an efficient use of the surface and bulk active sites, resulting in a relatively large Tafel slope (Tafel plots show the dependence of the rate of an electrochemical reaction on the overpotential). The mono- and di-μ-oxo-bridged Mn ions in 3D cross-linked structures resulted in a low intrinsic activity and a small Tafel slope, and, therefore, a favorable activity for artificial water splitting. This research group also reported an increase in the mean Mn oxidation state of Mn oxides upon operation at catalytic potentials.436 Such studies can be very important for the clarification of the mechanism of water oxidation catalyzed by Mn oxides. Nørskov proposed that in the individual stages of the wateroxidation process, interactions of intermediates with the surface are observed (e.g., *OH, *O, and *OOH, where “*” denotes bonding to the surface).485−487 Reaction stages such as the formation of *OH/*O from H2O are assisted by stronger

interactions of O atoms with the surface. Nevertheless, other subprocesses, including: *O + H 2O(l) → OOH−(aq) + H+(aq) + e−

may be less favored, as the surface−oxygen bonds are ruptured.486,487 Such a trade-off results in optimum values for the surface−oxygen interaction energies, which maximize the general rate (volcano shape). As postulated by Nørskov, this description is in accordance with Sabatier’s rule, which states that the interaction between the catalyst and the adsorbate should not be too strong or too weak.488 Other groups also noted the importance of eg orbitals for the catalytic activity of metal oxides in water oxidation. Maitra et al.489 reported that oxides with a cation that has a d4 or a d6 configuration, with one electron in an antibonding eg orbital, show high catalytic activities for water oxidation, irrespective of the crystal structure of the catalyst. The eg orbital can form σ bonds with anionic adsorbates, and it can influence the binding of oxygen-related intermediates to the catalyst during electrochemical oxygen evolution and oxygen reduction reactions.489 Vojvodic and Nørskov490 showed that there is a similar correlation between water oxidation and t2g orbital population. The occupied eg and t2g orbitals were shown to provide two relevant contributions: one from the populated valence-band states and one from the populated conductionband states. As a result of the surface interaction with Oadsorbate levels, bonding and antibonding O states arise.490 The population of these states affects the adsorption strength. Complete occupation of the O-bonding states without occupation of the antibonding states results in the strongest interaction. The adsorbate and the metal surface are involved in a bonding interaction, with the d-band metal center as a parameter.490 Dau et al.13 reviewed the mechanistic aspects of the water oxidation catalyzed by transition metal complexes. Interestingly, it was reported that many Mn oxides (Mn3O4, αMn 2 O 3 , β-MnO 2 , CaMnO 3 , Ca 2 Mn 3 O 8 , CaMn 3 O 6 , and CaMn4O8) convert into layered Mn oxides after several hours during the water-oxidation reaction in the presence of CAN. The researchers proposed that, depending on the conditions of water oxidation, Mn-based catalysts transform into a Mn oxide phase (usually a layered structure) that can be predicted by a Pourbaix diagram and that represents the true catalyst for water oxidation.472 Recently, Indra et al.473 considered the reaction of MnO with CAN. They reported that treatment with CAN transforms MnO into a layered Mn oxide; the layered form is an active catalyst for water oxidation. Thus, considering these results, finding precatalysts as well as catalysts is an important 2920


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ducted in serial time-resolved crystallography of PSII helped to reveal some new facts. Specifically, the structure of the dark S1 state (5 Å resolution) could be differentiated from the S3-state structure (5.5 Å resolution). Changes in the protein surroundings and conformation of the Mn4CaOx cluster were proposed; these changes may enable the binding of an additional water ligand between the protruding Mn atom and the Mn3CaOx core in the S2 → S3 transition.185 Even though not all strategies used by nature in photosynthesis may be readily applicable for industrial applications, discovering how these strategies give rise to the “art” of water oxidation by nature will open new approaches for the design of bioinspired catalysts. Incorporating the catalyst in the form of a nanosized oxido cluster, using channels (as seen in PSII), and considering other factors (such as the outer hydrogen bonds, the spin-flipping rule, redox accumulation in the WOC, regulating oxidizing power, the photosystem’s ability for self-repair, and various strategies used to protect the active site) may provide valuable insights into the future design of robust artificial water-oxidizing compounds. To obtain a successful catalyst for water oxidation, the longterm stability of the catalyst must also be carefully considered. Many Mn complexes, including Mn oxides, convert into other materials under the conditions required for water oxidation. Further, there are no chemical groups near the active sites in Mn oxides that can regulate the charge, electrochemistry, proton transfer, etc. Therefore, a future goal is to design or engineer Mn (or other metal) oxides to have such groups. To this end, experimental approaches and theoretical calculations aimed at clarifying the mechanism and important factors that affect the catalyst’s efficiency are of key importance to the design of efficient, inexpensive, environmentally friendly, and stable catalysts for water oxidation.

issue, not only for molecular water-oxidizing complexes but also for metal oxides. Another important point to compare water-oxidizing activities of Mn oxides was recently reported by Stahl’s research group. These researchers found that the identity of the “best” catalyst among different Mn oxides toward water oxidation depends on the oxidation method used to probe the catalytic activity.491 Also, recently, photoelectrochemical performance of MnOx toward the water-oxidation reaction was considered by the groups of Spiccia and MacFarlane.492 Their results show that (i) the wateroxidation rate on MnOx can be improved by illumination, and in the presence of buffered amine ionic liquid, H2O2 production can be observed; (ii) the photocurrent generation can be partly attributed to decomposition of H2O2 under light; (iii) the optimum photocurrent values are achieved on a MnOx layer with thickness of 4 μm; and (iv) the photocurrent is linearly dependent on the light intensity.

9. IMMOBILIZATION OF PSII ON THE SURFACE OF ELECTRODES Another approach to the oxidation of water is the extraction of PSII and its immobilization on the surface of electrodes.493−496 These PSII-coated electrodes could act as heterogeneous catalysts for water oxidation. Under illumination, the system could promote the water-splitting process at oxidation potentials of ca. 0 V vs NHE. Nevertheless, PSII has a limited operational stability when exposed to light. Recently, the Reisner group proved that PSII can be covalently linked to a mesoporous indium tin oxide electrode functionalized with carboxylate groups to give a catalyst for visible-light-driven water oxidation, having a TOF of 0.61 ± 0.12 s−1 for oxygen evolution.494,495 10. NON-BIOMIMETIC WATER-OXIDIZING CATALYSTS The design and synthesis of water-oxidizing catalysts using strategies, chemicals, and methods that are not based on the WOC are also very interesting.497,498 Synthetic catalysts (e.g., nickel oxide in alkaline electrolyzers and iridium oxide in protonexchange membrane electrolyzers) operate at high current densities (1 A cm−2) without deactivation on a time scale of years. In this context, efficient catalysts based on metals other than Mn and with high TOFs, containing Fe (0.25−1.3 s−1),499,500 Ni (0.015 s−1),501 Co (5 s−1),502 Ru (>300 s−1),503 and Ir (1.5 s−1),504 were reported by some groups. These wateroxidizing catalysts based on metals other than Mn are very promising for use in artificial photosynthetic systems. However, learning from PSII remains of great importance, because these photosystems have been successfully splitting water for millions of years, using an inexpensive and environmentally friendly Mn− Ca oxido cluster.

AUTHOR INFORMATION Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Notes

The authors declare no competing financial interest. Biographies Mohammad Mahdi Najafpour received his Ph.D. in Inorganic Chemistry from Sharif University of Technology, Tehran, Iran, in 2009. Mahdi is a recipient of several awards and fellowships, notably the gold medal of the National Chemistry Olympiad in 2004. In addition, he ranked 1st in the Khwarizmi Youth Festival in 2010, and he was selected for the TWAS young affiliateship (2014). Mahdi also received the AlBiruni award by the Academy of Sciences of Iran (2015), and he was selected to be among the best researchers in Iran by the Ministry of Science of Iran (2015). Currently, he is a faculty member in Chemistry in the Institute for Advanced Studies in Basic Sciences (IASBS) (Zanjan, Iran). As a nanobioinorganic chemist, Mahdi believes that with learning strategies from natural systems, design of modern catalysts for all reactions using only Earth abundant, low cost, and environmentally friendly metal ions is possible. Mahdi and his research group explore transition-metal compounds as water-oxidizing catalysts for artificial photosynthesis. He is the author of over 160 publications in these and other areas.

11. BRIEF CONCLUDING REMARK Photosystem II is the only water-oxidizing enzyme in nature. In this Review, we discussed the most important issues regarding water oxidation catalyzed by the enzyme and related artificial Mn-based functional models. During the past decade, studies of the structural as well as mechanistic aspects of water oxidation by PSII were recognized to provide a roadmap for the design, synthesis, and application of efficient water-oxidizing compounds for artificial photosynthetic systems. However, to find out more about photosynthesis, we also need new devices and techniques. X-ray free-electron lasers (XFELs) seem to be the key to future structural investigations on PSII. Recently experiments con-

Gernot Renger (1937−2013) obtained his doctoral degree, in 1970, in the research group of Professor Horst Witt at the Max-VolmerLaboratory at the Technical Universtity (TU) in Berlin, Germany. His thesis project, which remained his scientific passion throughout his 2921


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University of Tokyo. He also worked as a visiting research associate of the Department of Chemistry at the University of North Carolina at Chapel Hill (1987−1989), and as a researcher of PRESTO, JRDC (1992−1996). His research has been focused on the creation of new electro- and photofunctional materials comprising both transition metals and p-conjugated chains, and invention of unidirectional electron-transfer systems utilizing molecular layer interfaces.

career, concerned the mechanism of photosynthetic water oxidation, which back then was basically a black box that he studied by lightinduced oxygen evolution. After his habilitation in 1977, he soon became full professor of Physical Chemistry, in 1980, at the TU in Berlin, where he worked beyond his retirement (2003) until the evening before his unexpected death on January 12, 2013. His scientific work covered nearly all areas of the primary processes in photosynthesis. He made tremendous contributions, especially regarding the elucidation of the kinetics and thermodynamics of photosynthetic water oxidation. Gernot Renger has authored more than 400 scientific publications. We miss him and his thought-provoking questions and congenial friendship at international meetings.

Julian J. Eaton-Rye is a Professor in the Department of Biochemistry at the University of Otago, New Zealand. He received his Ph.D. from the University of Illinois in 1987, where he worked with Govindjee on the role of bicarbonate in the regulation of electron transfer through Photosystem II. Before joining the Biochemistry Department at Otago University in 1994, he was a postdoctoral researcher focusing on various aspects of Photosystem II protein biochemistry with Professor Norio Murata at the National Institute of Basic Biology in Okazaki, Japan; with Professor Wim Vermaas at Arizona State University; and with Dr. Geoffrey Hind at Brookhaven National Laboratory. His current research interests include structure−function relationships of Photosystem II proteins as well as the role of additional protein factors in the assembly of Photosystem II.

Małgorzata Hołyńska received her Ph.D. degree from Wrocław University (Poland) in 2009. Subsequently, she completed a one-year postdoctoral research stay as an Alexander von Humboldt fellow in the group of Prof. Dr. Stefanie Dehnen at Philipps-University Marburg (Germany). Since then she continues her independent academic career as a junior research group leader (habilitation in 2014) at the same university. Her research interests include the chemistry of polynuclear metal complexes with oxime/Schiff-base ligands as new magnetic materials and for biological/catalytic applications, in particular as gene transfer agents and as precursors of new water-oxidation catalysts.

Jian-Ren Shen is a Professor and the Director of the Photosynthesis Research Center, Graduate School of Natural Science and Technology, Okayama University in Japan. He received his bachelor’s degree in Biology from Zhejiang Agricultural University (now Zhejiang University) in China in 1982 and gained his Ph.D. in Biochemistry from the University of Tokyo in 1990. He subsequently spent 13 years in RIKEN (The Institute of Physical and Chemical Research) in Japan with the group of Yorinao Inoue studying the structure and function of Photosystem II, and moved to Okayama University as a Professor in 2003, where he is continuing studies on the mechanism of photosynthetic water oxidation based on structural analysis of Photosystem II. In collaboration with his colleagues, he solved the structure of Photosystem II at 1.9 Å in 2011, which was selected as one of the “Breakthroughs of the Year 2011” by the journal Science. His research interests include the structure and function of Photosystem II, the wateroxidizing complex, catalytic conversion of solar energy, and highresolution crystal structural analysis of membrane proteins and their complexes.

Atefeh Nemati Moghaddam received her B.Sc. in Chemistry from the University of Tabriz in 2008. In 2012, she joined Dr. Najafpour’s research group as a M.Sc. student at the Institute for Advanced Studies in Basic Sciences. Her major research interest is water oxidation by Mnbased catalysts, and she has had 10 publications in the field. Atefeh also received an award for her research presentation on a “mathematical model for manganese oxide-coated clay as catalysts for water oxidation” at the international conference on Photosynthesis Research for Sustainability held in Baku, Azerbaijan in 2013. Eva-Mari Aro is an Academy Professor working in the Department of Biochemistry, University of Turku. She has published over 250 peerreviewed scientific papers, mostly on biophysics, biochemistry, and molecular biology of the photosynthetic apparatus. Aro has chaired the Academy of Finland Center of Excellence (AFCoE) “Integrative photosynthesis, bioactive compound and biohydrogen research” (2008−2013) and is currently chairing the AFCoE “Molecular biology of primary producers” 2014−2019. Aro is a partner and coordinator of several EU and Nordic research networks, and also a partner of an Australian CoE on Plant Energy Biology. Between 2004−2010 she served as president and past president of the International Society of Photosynthesis Research. Aro was vice chair of the Finnish Academy of Science and Letters 2012−2014 and is currently chair 2014−2016. She has many research- and science policy-related international duties of trust. She serves on the Science Advisory Boards of the Max Planck Institute (Golm) and the Dutch Government Program “BioSolarCells”.

Suleyman I. Allakhverdiev is the Head of the Controlled Photobiosynthesis Laboratory at the Institute of Plant Physiology of the Russian Academy of Sciences (RAS), Moscow; Chief Research Scientist at the Institute of Basic Biological Problems RAS, Pushchino, Moscow Region; Professor at M.V. Lomonosov Moscow State University, Moscow, Russia; and Invited-Adjunct Professor at the Department of New Biology, Daegu Gyeongbuk Institute of Science & Technology (DGIST), Daegu, Republic of Korea. He is originally from Chaykend (Karagoyunly/Dilichanderesi), Armenia, and he obtained both his B.S. and M.S. in Physics from the Department of Physics, Azerbaijan State University, Baku. He obtained his Dr. Sci. degree (highest/top degree in science) in Plant Physiology and Photobiochemistry from the Institute of Plant Physiology, RAS (2002, Moscow), and Ph.D. in Physics and Mathematics (Biophysics), from the Institute of Biophysics, USSR (1984, Pushchino). His Ph.D. advisors were Academician Alexander A. Krasnovsky and Dr. Sci. Vyacheslav V. Klimov. He worked for many years (1990−2007) as a visiting scientist at the National Institute for Basic Biology (with Prof. Norio Murata), Okazaki, Japan, and in the Department de Chimie-Biologie, Université du Québec at Trois Rivières (with Prof. Robert Carpentier), Québec, Canada (1988−1990). He has been a guest editor of many (more than 30) special issues in international peer-reviewed journals. At present, he is a member of the Editorial Board of more than 15 international journals. Besides being editor-in-chief of SOAJ NanoPhotoBioSciences, associate editor of the

Robert Carpentier is Professor at Universite du Québec a Trois-Rivières, Québec, Canada. He obtained his Ph.D. in biochemistry from Laval University (1983, Québec). He is editor of the Journal of Photochemistry and Photobiology B: Biology, associate editor of Photosynthesis Research, and was the chair of the XIIIth International Congress on Photosynthesis (Montreal, 2004). His research interests concern the influence of environmental stresses on electron transport pathways in Photosystems I and II, and energy dissipation in photosynthesis. Hiroshi Nishihara received his B.Sc. degree in 1977, M.Sc. in 1979, and D.Sc. in 1982 from the University of Tokyo. He was appointed research associate of the Department of Chemistry, Faculty of Science and Technology at Keio University in 1982, and he was promoted Lecturer in 1990, and Associate Professor in 1992. Since 1996, he has been a Professor of the Department of Chemistry, School of Science at the 2922


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PT QA QB QM/MM OEC RC ROS SEM SHE Si

International Journal of Hydrogen Energy, section editor of BBA Bioenergetics, he also acts as a referee for major international journals and grant proposals. He has authored (or coauthored) more than 350 research papers and 7 books. He has organized several (more than 10) international conferences on photosynthesis. His research interests include the structure and function of Photosystem II, the Photosystem II water-oxidizing complex, artificial photosynthesis, hydrogen photoproduction, catalytic conversion of solar energy, plants under environmental stress, and photoreceptor signaling.

ACKNOWLEDGMENTS M.M.N. and A.N.M. are grateful to the Institute for Advanced Studies in Basic Sciences and the National Elite Foundation for financial support. E.-M.A. and J.-R.S. were supported by the Academy of Finland (no. 118637) and by a grant-in-aid for Specially Promoted Research (no. 24000018) from JSPS, MEXT, Japan, respectively. This work was also supported by a grant from the Russian Science Foundation (no. 14-14-00039) to S.I.A. We thank Johannes Messinger for his helpful comments. We also would like to thank the following colleagues for preparing electronic versions of the figures: Bronwyn Carlisle, Susanne Renge, Jan Kern, Philipp Kühn, Athina Zouni, Jörg Pieper, Franz Josef Schmitt, and Davood Jafarian Sedigh. M.H. acknowledges Prof. Dr. Stefanie Dehnen and Prof. Dr. Florian Kraus for generous support.

TEM Terpy TON TOF UV−vis WOC XANES XES XRD XPS YD YZ

DEDICATION This Review is dedicated to the memory of Prof. G. Renger, who passed away on January 12, 2013.

proton transfer primary plastoquinone electron acceptor of PSII secondary plastoquinone electron acceptor of PSII quantum-mechanical/molecular-mechanical O2-evolving complex reaction center reactive oxygen species scanning electron microscopy standard hydrogen electrode notation for the oxidation states of the WOC (i = −3 to 4) transmission electron microscopy 2,2′:6′,2″-terpyridine turnover number turnover frequency ultraviolet−visible water-oxidizing complex X-ray absorption near-edge structure X-ray emission spectroscopy X-ray diffraction X-ray photoelectron spectroscopy redox-active tyrosine of the D2 RC protein (D2Y160) redox-active tyrosine of the D1 RC protein (D1Y161)

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ABBREVIATIONS AFM atomic force microscopy AMO amorphous manganese oxide BSA bovine serum albumin BQ p-benzoquinone CNTs carbon nanotubes COX cytochrome c oxidase Chl chlorophyll D1 reaction center protein of PSII D2 reaction center protein of PSII DFT density functional theory EDX energy-dispersive X-ray spectroscopy ET electron transfer ENDOR electron−nuclear double resonance EET excitation energy transfer EPR electron paramagnetic resonance EXAFS extended X-ray absorption fine structure FTIR Fourier transform infrared spectroscopy FTO fluorine doped tin oxide HRTEM high-resolution transmission electron microscopy H2BQ hydroquinone m-CPBA m-chloroperbenzoic acid meV millielectronvolt MS-PET multiple-site proton and electron transfer MIMS membrane-inlet mass spectrometry NET nonadiabatic electron transfer NHE normal hydrogen electrode NMR nuclear magnetic resonance P680 PSII reaction-center pigments PCET proton-coupled electron transfer Pheo pheophytin PS photosystem 2923


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