Unveiling the Reactivity of a Synthetic Mimic of the ... - ACS Publications

Letter pubs.acs.org/JPCL

Unveiling the Reactivity of a Synthetic Mimic of the Oxygen Evolving Complex Umberto Raucci,† Ilaria Ciofini,‡,§ Carlo Adamo,*,§,∥ and Nadia Rega*,†,⊥ †

Dipartimento di Scienze Chimiche, Università di Napoli Federico II, Complesso Universitario di M. S. Angelo, via Cintia, I-80126 Napoli, Italy ‡ Laboratoire d’ Electrochimie, Chimie des Interfaces et Modelisation pour l’ Energie, CNRS UMR-7575, Chimie ParisTech, 11 rue P. et M. Curie, F-75231 Paris Cedex 05, France § Ecole Nationale Supérieure de Chimie de Paris, Chimie ParisTech, 11 rue P. et M. Curie, F-75231 Paris Cedex 05, France ∥ Institut Universitaire de France, 103 Bd Saint-Michel, F-75005 Paris, France ⊥ Italian Institute of Technology, IIT@CRIB Center for Advanced Biomaterials for Healthcare, Largo Barsanti e Matteucci, I-80125 Napoli, Italy S Supporting Information *

ABSTRACT: We simulated for the first time the oxygen−oxygen bond formation in a synthetic calcium-tetra manganese complex recently developed by Zhang and co-workers. In spite of promising structural similarities to the native oxygen evolving complex (OEC) in Photosystem II, several uncertainties on the mimic stability in water and on its potential catalytic activity still persist. Here, we characterized at density functional theory level the electronic and structural features of the Sn states of the complex, along with the oxygen− oxygen bond formation reaction, proposing a reasonable model for the hydrate complex. As a main finding, both the synthetic compound and the natural OEC show very close energetic barriers for the oxo-oxyl coupling process, suggesting that key electronic features of the natural OEC reactivity are well reproduced. This result strongly encourages the use of this synthetic complex in combination with other molecular assemblies for the design of successful artificial leaves.

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being devoted to provide efficient and stable WOCs, and both heterogeneous and homogeneous molecular metal oxide WOCs have been reported.12,13,15 The performances of molecular WOCs can be tuned through the choice of transition metal nature, oxidation state and coordination, and, overall, through structural modifications of the surrounding ligands in order to increase the solubility of the molecular complex and to enable its anchoring to the electrode. Moreover, the mechanistic characterization of molecular WOCs is easier to achieve when compared to that of heterogeneous ones. For all these reasons, many researchers are working to develop molecular WOCs operating in homogeneous solution.12,13 Of course, Mn represents the exemplary element for wateroxidizing chemistry considering its fundamental role in PSII. Several manganese-based complexes have been proposed in the past decade, but only a few are effectively capable of catalyzing water oxidation.13,16−18 Taking inspiration from PSII, its oxygen evolving complex (OEC) can be the turning point for the design and synthesis of successful WOCs.

he development of successful photoelectrochemical cells to convert solar into chemically accessible energy relies on the efficiency in harvesting sunlight and storing its energy into chemical bonds.1−7 The award for the best efficient nanotechnology goes, of course, to Nature for the Photosystem II (PSII). As a matter of fact, the efficiency of PSII in using solar photons to activate the highly thermodynamically unfavored reaction of water oxidation to dioxygen is amazing:8−10 + − 2H 2O(l) → O2(g) + 4H(l) + 4e(g)

A standard redox potential of 1.23 V is associated with this reaction,11 which requires the extraction of four protons and four electrons together with the formation of an oxygen− oxygen bond. PSII represents the best inspiration when developing artificial leaves by using molecular assemblies for light energy conversion.3,7,10 Over time, a large number of molecules that mimic one or more elements of PSII have been evolved in order to build up a complex supramolecular architecture able to carry out the artificial photosynthesis.3,5,12−14 Artificial reaction centers participate in the electrons/protons removal, while the O−O bond formation occurs thanks to the water oxidation catalyst (WOC). At the state of the art, the four electron water oxidation reaction represents the weak point for the development of competitive water splitting cells. Currently, huge efforts are © XXXX American Chemical Society

Received: September 19, 2016 Accepted: November 14, 2016

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waves in the cyclic voltammogram. Moreover, absorption spectra of complex A upon water titration in acetonitrile solution show that its structure is changing, maybe through labile ligands exchange, but no data clearly demonstrated this hypothesis. In this context, a theoretical approach becomes an essential tool to characterize the structures of the various Sn redox intermediates in the presence of water ligands and the performances of the complex in the activation of the O−O bond formation. This was the primary aim of the present work. In order to disentangle the reactivity of complex A in the presence of water, we proposed a model in which some of its ligands have been selectively exchanged with water molecules. These were arranged in such a way to reproduce the position of the native OEC crystallographic water molecules. Indeed, the crystallographic data of the natural OEC reveal the presence of four water molecules bound to the [Mn4CaO4] core (Figure 1). Two water molecules are bound to the Ca, and the other two to the dangling Mn4. Hence, starting from complex A, the ButCO2H, ButCO2− and pyridine ligands were exchanged with five water molecules to simulate the O−O bond formation (Figure 3), according to the following reaction:

In this direction, very recently Zhang and co-workers proposed a calcium tetra-manganese complex [Mn4CaO4(ButCO2)8(ButCO2H)2(py)] (But, tert-butyl; py, pyridine), hereafter named complex A, structurally related to the native OEC in PSII (see Figure 1).19

[Mn4CaO4 (Bu t CO2 )8 (Bu t CO2 H)2 (py)] + 5H 2O→ [Mn4CaO4 (Bu t CO2 )7 (Bu t CO2 H)(H 2O)5 ] + Bu t CO2 H + Bu t CO−2 + py Figure 1. Crystal structures of the native OEC and the synthetic complex A. The CaMn4 core is also represented. The native OEC structure is taken from pdb ID 3ARC.20

More closely, the pyridine ligand bound to Mn4 and the ButCO2− anion (bridging Mn4 and Ca) were substituted with three water molecules, two of which directly coordinate the Mn4, while the last one is bound to the calcium. The coordination sphere on the Ca atom was completed exchanging the ButCO2H acid ligand bridging the Ca and the oxygen atom labeled as O2 (Figure 1) with two further water molecules in such a way to preserve the hydrogen bond between the acid and the O2 center. After each ligand substitution, the structure was fully optimized in the S1 state considering the highest spin solution. Full geometry optimizations were performed at the UB3LYP23,24 level of theory adopting the LANL-2DZ basis set for Mn and Ca, 6-31G(d) for N and O, and 6-31G for C and H. The polarizable continuum model in its conductor-like version (CPCM) was adopted to represent the acetonitrile bulk solvation effects.25,26 All calculations have been performed using the Gaussian 09 program.27 The pentahydrate complex results less stable of about 4 kcal/ mol when compared to the synthetic one. This value is compatible with the replacement of a charge ligand (the acetate ion) with two neutral ones (water molecules) and the consecutive loss of charge−charge electrostatic interaction. It is reasonable to expect that the explicit representation of the solvation around the water ligands may increase the stability of the hydrate form. Table S1 of the Supporting Information (SI) summarizes the optimized Mn−Mn, Ca−Mn, and Mn−O distances for the complex A before and after the ligands exchange. The water molecules in the calcium coordination sphere induce an increase of the Ca−Mn distances. Indeed, upon the hydration, the Ca−Mn1, Ca−Mn3, and Ca−Mn4 distances elongate of 0.10, 0.14, and 0.09 Å, respectively. A minor effect involves the Mn4−O5 distance, which decreases of 0.04 Å.

Indeed, crystallographic data for complex A reveal a [Mn4CaO4] core, with a dangling Mn ion bound to a [Mn3CaO4] cubane, resembling the natural OEC structure. The connectivity of the Ca to the Mn ions is identical in the two cases. However, some differences with respect to the OEC appear: the μ2 oxo bridge, linking Mn3 and Mn4 in the native OEC, is replaced by a bridging carboxylate group in complex A and, most importantly, the water molecules coordinated to Mn4 and Ca ions are replaced by other ligands (Figure 1). Experimental data also suggest oxidation states of Mn3+ 1 , 4+ 3+ Mn4+ 2 , Mn3 , Mn4 (see Figure 1 for labels) for the synthesized complex, in complete analogy to the S1 state of the natural OEC.19 In spite of these encouraging structural similarities, several issues on the water-oxidizing chemistry of this mimic are still open. On one hand its electronic flexibility, namely, the capability to store oxidizing equivalent through the Mn oxidation, has to be univocally demonstrated yet. This represents a unique feature of the native OEC, whose reaction cycle comprises several distinct redox intermediates, the Sn states, defined by the oxidation state of the four manganese ions. By means of cyclic voltammetry, it was shown that complex A can undergo a sequential one electron oxidation. However, further analyses, for example based on mass spectrometry data, could be helpful for the identification of the oxidation products, ruling out the possibility that other species (e.g., decomposition products) could activate the water splitting process.21,22 On the other hand, no information is available on the structure of complex A in the presence of water. It has been experimentally observed that the addition of water to the mimic leads to obscured oxidation and reduction 5016

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Figure 2. Sn states involved in the O−O bond formation for complex A.

Figure 3. Structure of the complex A before and after the ligands exchange.

These findings resemble what was already observed for the native OEC, for which it is postulated that the S2 state shows two different interconvertible structures with very similar energy.10,28−30 The two structures are characterized by an open cubane with the oxidation to Mn(IV) of the dangling Mn atom, and by a closed cubane with an oxidized Mn1, respectively. The open cubane structure is more stable by about 1 kcal/mol.10 Starting from the open S2 structure, the oxidation of Mn1 and the deprotonation of the hydroxo ligand occur in the S2 → S3 step (see Figure 5). The S3 state is characterized by all the Mn ions in the oxidation state (IV) with an oxo ligand bound to Mn4, resulting in a globally compact structure of the cubane core. Indeed the Mn−Mn, Ca−Mn and Mn−O distances, especially those involving Mn1 ion, decrease in the S2 → S3 step. Mn1−O3 and Mn1−O5 distances are shortened by 0.13 and 0.37 Å, respectively. Notably, the dangling Mn4 comes closer by about 0.15 Å to the oxygen of the water molecule (OW1) and farther away by about 0.11 Å from O5. A rearrangement in the opposite direction occurs in the S3 → S4 step, when the OW1 oxo ligand is oxidized, leading to the formation of an oxyl radical directly bound to the Mn4 ion (see S4 structure in Figure 4d). Three spin configurations were investigated for the S4 state, as shown in Figure S1 of the SI. In the high spin (HS) state, Mn ions and the oxyl radical are ferromagnetically coupled, while the low spin (LS) configuration is characterized by an antiferromagnetic coupling of the Mn atoms of the cubane core. The spin state with the oxyl ligand antiferromagnetically

The S1 state was considered as resting state (see Figure 2), while S2 and S3 states were obtained by the sequentially oxidation of the Mn(III) ions coupled with the deprotonation of the water directly bound to the Mn4 (W1 in Figure 3). For the S1, S2, and S3 states only the highest spin configuration was considered, while for the S4 state several spin configurations were investigated. The structures of S1, S2, S3, and S4 states are represented in Figure 4, while the atomic Mulliken spin densities are reported in Figure 5. Structural parameters of each state are collected in Table S2 of the SI. The S1 → S2 transition leads to the preferential oxidation of the Mn4 atom, stabilized by the hydroxo ligand obtained by the first deprotonation of W1. In particular, the oxidation of Mn4 is favored by about 3 kcal/mol compared to that of the Mn1 center. Regarding the structural analysis, the Mn1 oxidation leads to a more compact arrangement than that obtained when oxidizing Mn4. Indeed, upon the Mn4 oxidation the S2 structure is characterized by the lengthening of the Ca−Mn distances, while Mn−Mn and Mn−O distances show only slight changes. Specifically, Ca−Mn1, Ca−Mn2, and Ca−Mn4 distances change by about 0.05 Å, whereas Ca−Mn3 shows a marked variation going from 3.70 Å in S1 to 3.83 Å in S2. Instead, oxidation of the Mn1 center in the S1 → S2 step leads to a contraction of the CaMn3O4 core. In this case, Mn1−O1, Mn1−O3 and Mn1−O5 bond lengths are shortened by 0.01, 0.18, and 0.35 Å, respectively, compared to the S1 structure. This leads to a decrease of the Ca−Mn1 and Mn1−Mn3 distances. Nevertheless, in both the Mn1 and Mn4 oxidation, the hydroxide ion formed by the W1 deprotonation comes closer to the Mn4 ion, reaching roughly the same distance of about 1.80 Å. 5017

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Figure 4. Structure of the complex A in the S1, S2, S3, and S4 states. Structures of the transition state (TS) of the O−O bond forming step are also provided for the high (HS) and low (LS) spin states.

In the S4 state, the oxygen−oxygen bond formation takes place. Two mechanisms for the O−O bond formation are frequently considered in the photocycle of the OEC: water nucleophilic attack and oxyl-oxo coupling processes.9,31−37 The water nucleophilic attack involves a water molecule in the calcium coordination sphere, whose nucleophilicity increases after deprotonation by an arginine residue.32 On the other hand, the oxyl-oxo coupling mechanism occurs between an oxyl-radical and an oxo-oxygen inside the cubane core.9,35,37 This latter mechanism was considered in the present study (see Figure 6). In particular, the attack of the oxyl radical on the O5 atom of the cubane core was investigated. Transition states have been located for both the HS and LS spin configurations by the Synchronous Transit-Guided Quasi-

coupled to the ferromagnetically coupled Mn atoms (OA state) was also computed (Figure S1). The LS solution is more stable by about 6.70 kcal/mol with respect to the HS one, while the LS and OA states are nearly degenerate, with the OA solution more stable by 0.53 kcal/mol. From a structural point of view, the cubane core shows almost the same features in both LS and OA spin configurations (see Table S2). The distance between Mn4 and the oxyl radical is the main structural difference, being 0.10 Å longer in the HS configuration (see Table S2). On the other hand, the Mn4−O5 bond length remains almost unchanged. Globally, in the S4 state, the Mn4−OW1 bond length increases while the Mn4−O5 one decreases compared to the S3 state (Table S2). 5018

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Figure 5. Mulliken spin densities for Mn ions and OW1 of the CaMn4O4 core in the S1, S2, S3, and S4 states.

corresponding transition states. Mulliken spin densities for the HS and the LS solutions are provided in Figure S1. The computed barriers for the HS and LS solutions are 18.8 and 23.4 kcal/mol, respectively. These values can be compared with those computed by Siegbahn for the native OEC.37 Barriers of 19.3 and 25.9 kcal/mol are reported for the oxyl-oxo coupling process, respectively, for the HS and LS configuration.37 From a structural point of view the TS structures are characterized by an elongation of the Mn−O5 bonds. This effect leads, in turn, to an increase of the Mn−Mn distances. Moreover, in both the HS and LS solutions the Mn4−OW1 bond length reaches roughly the same value of about 1.77 Å at the transition state. At the same time, the OW1−O5 distance assumes a value of 1.76 and 1.77 Å in the HS and LS configurations, respectively (see Table S3). To conclude, our theoretical simulations investigated the hidden potentialities of the recently synthesized molecular complex A, which presents very promising energetic features for O−O bond formation. Indeed, both synthetic and natural OECs show very close energetic barriers for the oxo−oxyl coupling process, suggesting that the key electronic features of the natural OEC reactivity are well reproduced. This finding represents crucial information to promote complex A coupling to other molecular assemblies for the development of successful artificial leaves.

Figure 6. Schematic representation of the O−O bond formation mechanisms.

Newton method.38 The nature of the obtained structures was confirmed by the presence of a single imaginary frequency with value of 858i cm−1 and 736i cm−1 in the HS and the LS spin state, respectively. These values correspond to a mode mainly composed by a O−Mn−O bending where the two oxygen atoms move toward and away from each other (see Figure S2 for a representation of the displacement vectors), with an active participation of Mn4. Unfortunately, we were not able to locate the TS also for the OA solution. However, due to the structural and energetic similarities between the OA and the LS S4 states, we may reasonably hypothesize a resemblance also between the

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett.6b02144. Optimized Mn−Mn, Ca−Mn, and Mn−O distances (Å) for the S1 state of complex A before and after the ligands exchange; optimized structural parameters of the 5019

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Electron Transfer Chain in Photosystem II with a Molecular Triad Thermodynamically Capable of Water Oxidation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15578−15583. (15) Harriman, A.; Pickering, I. J.; Thomas, J. M.; Christensen, P. A. Metal Oxides as Heterogeneous Catalysts for Oxygen Evolution under Photochemical Conditions. J. Chem. Soc., Faraday Trans. 1 1988, 84, 2795−2806. (16) Mullins, C. S.; Pecoraro, V. L. Reflections on Small Molecule Manganese Models that Seek to Mimic Photosynthetic Water Oxidation Chemistry. Coord. Chem. Rev. 2008, 252, 416−443. (17) Kanady, J. S.; Tsui, E. Y.; Day, M. W.; Agapie, T. A Synthetic Model of the Mn3Ca Subsite of the Oxygen-Evolving Complex in Photosystem II. Science 2011, 333, 733−736. (18) Mukherjee, S.; Stull, J. A.; Yano, J.; Stamatatos, T. C.; Pringouri, K.; Stich, T. A.; Abboud, K. A.; Britt, R. D.; Yachandra, V. K.; Christou, G. Synthetic Model of the Asymmetric [Mn3CaO4] Cubane Core of the Oxygen-Evolving Complex of Photosystem II. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 2257−2262. (19) Zhang, C.; Chen, C.; Dong, H.; Shen, J.-R.; Dau, H.; Zhao, J. A Synthetic Mn4Ca-Cluster Mimicking the Oxygen-Evolving Center of Photosynthesis. Science 2015, 348, 690−693. (20) Umena, Y.; Kawakami, K.; Shen, J.-R.; Kamiya, N. Crystal Structure of Oxygen-Evolving Photosystem II at a Resolution of 1.9 Å. Nature 2011, 473, 55−60. (21) Ullman, A. M.; Liu, Y.; Huynh, M.; Bediako, D. K.; Wang, H.; Anderson, B. L.; Powers, D. C.; Breen, J. J.; Abruña, H. D.; Nocera, D. G. Water Oxidation Catalysis by Co (II) Impurities in Co (III) 4O4 Cubanes. J. Am. Chem. Soc. 2014, 136, 17681−17688. (22) Hocking, R. K.; Brimblecombe, R.; Chang, L.-Y.; Singh, A.; Cheah, M. H.; Glover, C.; Casey, W. H.; Spiccia, L. Water-Oxidation Catalysis by Manganese in a Geochemical-Like Cycle. Nat. Chem. 2011, 3, 461−466. (23) Becke, A. Density-Functional Exchange-Energy Approximation with Correct Asymptotic Behavior. Phys. Rev. A: At., Mol., Opt. Phys. 1988, 38, 3098−3100. (24) Becke, A. D. Density-Functional Thermochemistry. III. The Role of Exact Exchange. J. Chem. Phys. 1993, 98, 5648−5652. (25) Cossi, M.; Rega, N.; Scalmani, G.; Barone, V. Energies, Structures, and Electronic Properties of Molecules in Solution with the C-PCM Solvation Model. J. Comput. Chem. 2003, 24, 669−681. (26) Barone, V.; Cossi, M. Quantum Calculation of Molecular Energies and Energy Gradients in Solution by a Conductor Solvent Model. J. Phys. Chem. A 1998, 102, 1995−2001. (27) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A. et al. Gaussian 09, revision A.2; Gaussian Inc.: Wallingford, CT, 2009. (28) Pantazis, D. A.; Ames, W.; Cox, N.; Lubitz, W.; Neese, F. Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S2 State. Angew. Chem., Int. Ed. 2012, 51, 9935−9940. (29) Bovi, D.; Narzi, D.; Guidoni, L. The S2 State of the OxygenEvolving Complex of Photosystem II Explored by QM/MM Dynamics: Spin Surfaces and Metastable States Suggest a Reaction Path Towards the S3 State. Angew. Chem., Int. Ed. 2013, 52, 11744− 11749. (30) Isobe, H.; Shoji, M.; Yamanaka, S.; Umena, Y.; Kawakami, K.; Kamiya, N.; Shen, J.-R.; Yamaguchi, K. Theoretical Illumination of Water-Inserted Structures of the CaMn4O5 Cluster in the S2 and S3 States of Oxygen-Evolving Complex of Photosystem II: Full Geometry Optimizations by B3LYP Hybrid Density Functional. Dalton Trans. 2012, 41, 13727−13740. (31) Siegbahn, P. E. Quantum Chemical Studies of Manganese Centers in Biology. Curr. Opin. Chem. Biol. 2002, 6, 227−235. (32) Barber, J. Photosystem II: the Water Splitting Enzyme of Photosynthesis and the Origin of Oxygen in Our Atmosphere. Q. Rev. Biophys. 2016, 49, 1−21. (33) Sproviero, E. M.; Gascón, J. A.; McEvoy, J. P.; Brudvig, G. W.; Batista, V. S. Quantum Mechanics/Molecular Mechanics Study of the

[Mn4CaO4] core in S1, S2, S3, and S4 states; optimized structural parameters of the [Mn4CaO4] core in the S4 minimum energy and TS structures, in the high and low spin configurations; Mulliken spin densities for Mn ions of the CaMn4O4 core in the S4 state in acetonitrile solution, in the high and low spin configurations; displacement vectors for the mode corresponding to the imaginary frequency of high and low spin transition states; Cartesian coordinates of all the optimized structures (PDF)

AUTHOR INFORMATION

Corresponding Authors

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

Nadia Rega: 0000-0002-2983-766X Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS U.R. and N.R. acknowledge funds from Regione Campania (L.R. 5, BRC3179) REFERENCES

(1) Berardi, S.; Drouet, S.; Francàs, L.; Gimbert-Suriñach, C.; Guttentag, M.; Richmond, C.; Stoll, T.; Llobet, A. Molecular Artificial Photosynthesis. Chem. Soc. Rev. 2014, 43, 7501−7519. (2) Gust, D.; Moore, T. A.; Moore, A. L. Realizing Artificial Photosynthesis. Faraday Discuss. 2012, 155, 9−26. (3) Llansola-Portoles, M. J.; Palacios, R. E.; Gust, D.; Moore, T. A.; Moore, A. L. From Molecules to Materials; Springer: Cham, Switzerland, 2015; pp 71−98. (4) House, R. L.; Iha, N. Y. M.; Coppo, R. L.; Alibabaei, L.; Sherman, B. D.; Kang, P.; Brennaman, M. K.; Hoertz, P. G.; Meyer, T. J. Artificial Photosynthesis: Where Are We Now? Where Can We Go? J. Photochem. Photobiol., C 2015, 25, 32−45. (5) Kärkäs, M. D.; Johnston, E. V.; Verho, O.; Åkermark, B. Artificial Photosynthesis: from Nanosecond Electron Transfer to Catalytic Water Oxidation. Acc. Chem. Res. 2014, 47, 100−111. (6) Fujishima, A.; Honda, K. Photolysis-Decomposition of Water at the Surface of an Irradiated Semiconductor. Nature 1972, 238, 37−38. (7) Zhou, H.; Yan, R.; Zhang, D.; Fan, T. Challenges and Perspectives in Designing Artificial Photosynthetic Systems. Chem. Eur. J. 2016, 22, 9870−9885. (8) Barber, J. PhotosystemII: the Engine of Life. Q. Rev. Biophys. 2003, 36, 71−89. (9) Siegbahn, P. E. Water Oxidation Mechanism in Photosystem II, Including Oxidations, Proton Release Pathways, O−O Bond Formation and O2 Release. Biochim. Biophys. Acta, Bioenerg. 2013, 1827, 1003−1019. (10) Cox, N.; Pantazis, D. A.; Neese, F.; Lubitz, W. Artificial Photosynthesis: Understanding Water Splitting in Nature. Interface Focus 2015, 5, 9−18. (11) Pourbaix, M. Atlas of Electrochemical Equilibria in Aqueous Solutions; Pergamon Press: Oxford, U.K., 1966. (12) Blakemore, J. D.; Crabtree, R. H.; Brudvig, G. W. Molecular Catalysts for Water Oxidation. Chem. Rev. 2015, 115, 12974−13005. (13) Najafpour, M. M.; Renger, G.; Hołyńska, M.; Moghaddam, A. N.; Aro, E.-M.; Carpentier, R.; Nishihara, H.; Eaton-Rye, J. J.; Shen, J.R.; Allakhverdiev, S. I. Manganese Compounds as Water-Oxidizing Catalysts: From the Natural Water-Oxidizing Complex to Nanosized Manganese Oxide Structures. Chem. Rev. 2016, 116, 2886−2936. (14) Megiatto, J. D.; Antoniuk-Pablant, A.; Sherman, B. D.; Kodis, G.; Gervaldo, M.; Moore, T. A.; Moore, A. L.; Gust, D. Mimicking the 5020

DOI: 10.1021/acs.jpclett.6b02144 J. Phys. Chem. Lett. 2016, 7, 5015−5021

Letter

The Journal of Physical Chemistry Letters Catalytic Cycle of Water Splitting in Photosystem II. J. Am. Chem. Soc. 2008, 130, 3428−3442. (34) Siegbahn, P. E. An Energetic Comparison of Different Models for the Oxygen Evolving Complex of Photosystem II. J. Am. Chem. Soc. 2009, 131, 18238−18239. (35) Li, X.; Siegbahn, P. E. Alternative Mechanisms for O2 Release and O−O Bond Formation in the Oxygen Evolving Complex of Photosystem II. Phys. Chem. Chem. Phys. 2015, 17, 12168−12174. (36) Cox, N.; Retegan, M.; Neese, F.; Pantazis, D. A.; Boussac, A.; Lubitz, W. Electronic Structure of the Oxygen-Evolving Complex in Photosystem II Prior to O-O Bond Formation. Science 2014, 345, 804−808. (37) Siegbahn, P. E. O-O Bond Formation in the S4 State of the Oxygen-Evolving Complex in Photosystem II. Chem. - Eur. J. 2006, 12, 9217−9227. (38) Peng, C.; Schlegel, H. B. Combining Synchronous Transit and Quasi-Newton Methods to Find Transition States. Isr. J. Chem. 1993, 33, 449.

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