Mn4Ca Cluster of Photosynthetic Oxygen-Evolving Center: Structure

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The Mn4Ca-cluster of the photosynthetic oxygen evolving centre: its structure, function and evolution. James Barber Biochemistry, Just Accepted Manuscript • DOI: 10.1021/acs.biochem.6b00794 • Publication Date (Web): 05 Oct 2016 Downloaded from http://pubs.acs.org on October 9, 2016

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The Mn4Ca-cluster of the photosynthetic oxygen evolving center: its structure, function and evolution. James Barber Department of Life Sciences, Sir Ernst Chain Building, South Kensington Campus, Imperial College London, SW7 2AZ, UK Authors information Email: [email protected] Tel. No: + 44 20 8747 1165 Abbreviations: DFT Density Function Theory OEC Oxygen Evolving Center PSII Photosystem Two QM/MM Quantum Mechanical/Molecular Mechanical XAFS X-ray Absorption Fine Structure XFEL X-ray Free Electron Laser

Running title: “The Mn4Ca-cluster of Photosystem II” Keywords: Photosynthesis, Manganese cluster, Photosystem II, Cubane Model, Structure, Water Splitting, Oxygen Evolving Center. Contents. Abstract. 1. Mechanism of water splitting and O-O bond formation. 2. Amino Acid ligands. 3. Chemical synthesis of OEC mimics. 4. Natural Mn oxide minerals Conclusions. Acknowledgements. References.

Abstract Photosystem II is the chlorophyll containing enzyme in which the very first chemical energy storing reaction of photosynthesis occurs. It does so by splitting water into molecular oxygen and hydrogen equivalents at a catalytic center composed of four Mn ions and one Ca2+. All the oxygen in the atmosphere is derived from this reaction and without it the biosphere, as we know it, would not exist. Indeed, the appearance of this catalytic center about 3 billion years ago gave rise to the “big bang of evolution”. Thus understanding the structure and functioning of this metal cluster is a major topic in science and here I discuss it in terms of research which has occurred over of the last twelve years dating back to when it was first proposed to be a Mn3CaO4 cubane with the fourth Mn attached to cubane by one of its oxo bridging bonds. Since then a number of novel properties have emerged for this metallo-protein with implications for its catalytic mechanism and evolutionary origin.

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Powered by sunlight, Photosystem II (PSII) supplies biology with the ‘hydrogen’ (reducing equivalents) needed to convert carbon dioxide into organic molecules while at the same time generating the oxygen of our aerobic atmosphere. Its appearance during evolution dramatically changed the chemical composition of our planet and set in motion an unprecedented explosion in biological activity resulting in the establishment of the global biosphere and laying down of fossil fuels. It has long been known that the catalytic water splitting site contains four Mn ions (1), and understanding their organisation and interaction during catalysis of water oxidation has been a “holy grail” of bioinorganic chemistry The importance of this cannot be over stated since splitting water into its elemental constituents is thermodynamically and chemically demanding and is accomplished by the relatively low energy content of four photons of visible light absorbed by chlorophyll (Equ.1). 2H2O 4 hν > O2 + 4e + 4H+…………………………………………………………(1) The four high energy electrons, together with 4H+, are used to reduce plastoquinone (PQ) , the terminal electron acceptor of PSII, to plastoquinol (PQH2) (Equ. 2). 4e + 4H+ + PQ 4 hν > 2PQH2. ………………………………………………….. (2) PQH2 passes its reducing equivalents to an electron transfer chain which feeds into Photosystem I (PSI) and gains the additional reducing potential from a second light reaction necessary to drive CO2 reduction (2). For many years it was agreed that there were four Mn ions in the catalytic center and that they function to accumulate the four oxidising equivalents necessary to split two water molecules and generate a molecule of dioxygen. That each photon absorbed drives each oxidation step at one catalytic center was cleverly shown by monitoring oxygen release in a series of single turnover flashes of light where the maximum yield of oxygen followed a period of four and gave rise to a scheme known as the S-state cycle (S0 to S4) (see Fig.1)(3,4)). A whole range of techniques, particularly magnetic resonance spectroscopy, have shown that each step in this cycle involves an increase in the oxidation of a Mn ion, starting at So with 3Mn (III) plus Mn(IV) advancing to S3 with 4 Mn(IV). The precise details of the final oxidation state, S4 , are unknown because O-O bond formation is very fast. This cycle is powered by the initial oxidation of a chlorophyll known as P680 generated by light driven primary charge separation in the reaction center of PSII coupled to a redox active tyrosine (Yz) serving as an intermediate electron carrier between P680+ and the Mncluster (see Fig. 1).


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Figure 1. The S-state cycle showing how the absorption of four photons of light (hν ν) by P680 drives the splitting of two water molecules and formation of O2 through a consecutive series of five intermediates (S0, S1, S2, S3 and S4). Protons (H+) are released during this cycle except for the S1 to S2 transition. Electron donation from the Mn4Ca-cluster to P680•+ is aided by the redox active tyrosine YZ . Each step involves a single oxidation of a Mn ion in the cluster, starting at So with 3Mn (III) plus Mn(IV) advancing to S3 with 4 Mn(IV). The exact oxidation state of S4 is unknown but could be 3 Mn(IV) plus Mn (V) or a Mn(IV)-oxyl radical (see below) Also shown are half-times for the various steps of the cycle.

Not surprisingly, it has been one of the greatest challenges of photosynthesis research to determine the structure of the Mn-containing cluster of the PSII oxygen evolving center (OEC) and reveal the molecular mechanism of the water splitting reaction. Such knowledge has far reaching implications for understanding the energy cycle of our planet and for the development of new technologies for the production of fuel (2). Over the years there have been many postulates of its structure mainly derived from X-ray absorption fine-structure (XAFS) spectroscopy (5) and electron paramagnetic resonance (EPR) studies (6,7). However, in 2004 a complete fully refined structure of PSII was determined at 3.5 Å resolution by X-ray crystallography by myself and colleagues at Imperial College London and published in Science (8). We were able to assign, for the first time, over 5000 amino acids side chains of this huge dimeric membrane complex (700kD) with each monomer consisting of 19 different protein subunits. In so doing we answered many outstanding questions as well as revealing a wide range of important details hitherto unknown. The native electron density map, together with anomalous diffraction data collected at wavelengths of 1.89 Å and 2.25 Å, provided electron density profiles for Mn and Ca2+ respectively. This information was then used to build a model of the metal-cluster. The anomalous electron density attributed to the four Mn ions was “pear-shaped” indicative of the 3 + 1 organisation and thus one Mn was assigned to the small domain and three in the large globular domain, whereas the 2.25 Å wavelength map covered one metal ion in the large domain of the native density. From this data the three Mn ions (Mn1, Mn2 and Mn3) and the Ca2+, located in the large domain, were modelled with a cubane geometry having bridging oxygens, an organisation which was compatible with the native electron density. The fourth Mn ion (Mn4), located in the small domain was modelled so that it was linked to the cubane by one of its bridging oxygens (see Fig 2A). Based on values determined by XAFS measurements and comparison with other Mn-containing proteins, the three Mn-di-μ-oxy-Mn bonds of the cubane were spaced at 2.7 Å while the three Mn-di-μ-oxy-Ca2+ bonds at 3.4 Å. The dangler Mn4 was positioned 3.3 Å from the closest Mn ion of the cubane and about 4 Å from the Ca2+. At that time there was no similar chemical structure known in biochemistry or chemistry and therefore the model was greeted with some uncertainty, especially since it had been conceived from relatively low resolution data. But the main opposition to this model was the argument that the metal cluster, and surrounding amino acid ligands, would be seriously disturbed by radiation damage during data collection. Indeed the cubane structure did not seem to be consistent with polarised XAFS measurements made at much lower radiation levels (9). Unfortunately, the claim that the Ferreira et al cubane model was invalid caused a substantial level of confusion, both for specialists and non-specialists. However it has become clear that the 2004 cubane model of Ferreira et al is valid within the limitation of its resolution and therefore the radiation damage argument and associated alternative postulated XAFS structures for the Mn-cluster(9) were totally wrong. Indeed, doubts in the interpretation of the polarized XAFS data were presented by Sproviero et al (10) who concluded that the polarized XAFS spectra were consistent with the cubane model which they went on to refine using QM/MM calculations. In 2011, seven years after the coordinates of the cubane model by Ferreira et al were deposited, the uncertainty of the cubane model was finally lifted with the report of 1.9 Å PSII structure from Umena et al (11). At this resolution the electron densities of individual metal ions could be resolved ACS Paragon Plus Environment

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and bridging oxygens inferred . As shown in Fig. 2B, the resulting model was overall similar to that of Ferreira et al (8) except an additional oxo bridge was identified linking the Mn outside the Mn3Ca-cubane (Mn4) to a Mn ion of the cubane.

Figure 2 (A) Comparison of the Mn4CaO4 cubane model from coordinates (PDB 1S5L) deposited by Ferreira et al in 2004 (8) with (B) the 1.9Å structure of the Mn4CaO5 cluster from Umena et al(11) and (C) the chemically synthesised Mn4CaO4-cubane by Zhang et al (25). Note that unfortunately, the numbering of the Mn and O are different in (B) and (C) to that originally given in (A).

Importantly this additional oxo-bridge had already been predicted by Dau et al (12) and particularly by Siegbahn (13) based on modification of the original 2004 cubane model using Density Function Theory (DFT) and other quantum mechanical methods (see Figure 5E). Nevertheless, the 1.9Å diffraction data of Umena et al (11), together with the data obtained by femtosecond X-ray freeelectron laser (XFEL) pulses (14) has provided a reliable atomic structure of the OEC, particularly in its dark-stable S1 state, which has allowed further detailed quantum mechanical calculations for the OEC and its functioning (15-21) and more rigorous interpretation of experimental results (22-24) Recently the PSII cubane cluster was synthesised as a Mn4CaO4 molecule (25) whose structure is remarkably similar to that proposed by Ferreira et al (8) (see Fig. 2C ). As with the Ferreira et al structure, the synthetic Mn4CaO4 molecule was also missing the additional oxo-bridge to Mn4. This insight into the structure of the catalytic center of PSII over the past twelve years gives rise to several important conclusions and novel discussions. 1. Mechanism of water splitting and O-O bond formation. The combination of DFT calculations and X-ray diffraction data has proved to be remarkably good for studying the OEC as emphasised by Siegbahn who predicted , using the Ferreira et al cubane model as the starting point, the existence and structure of the Mn4CaO5 cluster three years before the 1.9 Å crystal structure of Umena et al was published (Fig. 5E) (11). This powerful DFT approach has also been used extensively by Siegbahn (13,26) to explore the mechanism of water oxidation and particularly the nature of S4 in the S-state cycle . He concluded that the most likely mechanism is the formation of a terminal oxyl radical within the cubane at S4 which attacks a nearby bridging oxo to form the O-O bond (S4 to So transition) (see Fig.3A). This proposed mechanism has received some impressive experimental support (15,27). Recently the details of the S4 to S0 transition have been refined by Li and Siegbahn (28) to allow for conformational changes in and around the metal cluster but the general concept of an oxyl–oxo mechanism for O–O bond formation involves the same two manganese atoms and the central oxo group as in the original scheme described in Siegbahn’s 2008 paper (13) and earlier papers dating back to 2006 (26).


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Figure 3 (A) Mechanism 1. The formation of a terminal oxyl radical (13,25) originating from a substrate water incorporated during the S2 to S3 transition, leads to a radical attack of an adjacent oxo-ligand formed within the Mn3CaO4– cubane from the other substrate water during the establishment of the cubane geometry for the S0 state. (B) Mechanism 2. The very high oxidation state of the Mn-cluster, particularly the Mn ion outside the Mn3CaO5 cubane, leads to a high electron deficient oxo (after deprotonation of water molecules during the S-state cycle). Nucleophilic attack by water or a hydroxide of the second substrate water within the coordination sphere of Ca2+ leads to O2 formation.

Alternatively a well championed mechanism for photosynthetic dioxygen formation suggests that a substrate water, associated with Mn4, is deprotonated during the S-state cycle and converted to a highly electrophilic oxo (see Fig 3B) (29-32). This mechanism is dependent on Mn4 being converted to a high oxidation state (possibly Mn(V) or a very reactive Mn(IV)- oxyl radical) during progression to the S4-state just prior to O-O bond formation. The other three Mn ions are also in high valency states Mn(IV), Mn(IV), Mn(IV) at this stage and act as a further “oxidising battery” for the Mn(V)oxo or Mn(IV)-oxyl radical species on Mn4. In this way the reactive oxo linked to Mn4 is electron deficient, so much so that it makes an ideal target for a nucleophilic attack by the oxygen of the second substrate water bound within the coordination sphere of the Ca2+ (see Fig.4B). The deprotonation of the substrate waters would be aided by nearby bases such as CP43Arg357 and by the weak Lewis acidity of Ca2+. Indeed, there is an extensive H-bonding network leading from Yz to the lumenal side of OEC (11). However, according to Siegbahn this mechanism is not energy favourable compared to his oxo-oxyl mechanism (13,26) although the structure of the OEC and surrounding amino acids are consistent with this mechanism as emphasised by Ferreira et al (8). Moreover it does not require any large conformational changes involving oxo-bridge breakage of the cubane so that the chemistry is restricted to the surface of the metal cluster. 2. Amino Acid ligands The Ferreira et al structure (8) identified seven amino acids as ligands to the Mn4Ca-cluster, six from the D1 reaction center protein: Asp170, Glu189, His332, Ala344, Glu333 and Asp342 and Glu354 of the inner antenna chlorophyll-binding protein, CP43. That these seven amino acids are ligated to the Mn4Ca-cluster has been confirmed in the 1.9 Å structure of Umena et al (11) and the precise details of the ligation pattern revealed (see Fig. 4). The coordination properties of the three Mn ions of the cubane are totally satisfied by amino acid ligands. However, Umena et al (11) assigned two water ligands for non-cubane Mn4 and for the Ca ion as shown in Fig.4.


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Figure 4 Diagramatic representation of the amino acid side chains acting as ligands to the Mn4CaO5 cluster of the OEC together with four water molecules providing ligands to Ca and Mn4 (constructed from Umena et al crystal structure (11)). D1 residues shown in orange and green depict the CP43 residue Glu354.

Ferreira et al (8) also suggested that water molecules could act as ligands to Mn4 and Ca2+ and that this could be the site for dioxygen formation. The amino acids which serve as ligands to the metal cluster are highly conserved in PSII over the whole cynabacterial, plant and algal kingdoms (33). Yet there are a large number of reports that their replacement by other residues using site directed mutagenesis does not inhibit oxygen evolution completely and sometime not at all (34). One example is the replacement of the negatively charged D1-Glu189 by positively charged Lys which made no difference to the rate of oxygen evolution (35). This was also true for other D1-Glu189 mutants leading to the logical conclusion that it cannot be a ligand to the MnCa-cluster (35). Another example is the replacement of acidic CP43-Glu354 by neutral glutamine where O2 evolution persisted at a reduced rate of 1018% compared to the wild type(36). It is also possible to totally remove CP43 and yet assemble the OEC(37). Thus compared to many other metallo-enzymes, the assembled Mn4CaO5 cluster is rather robust to changes in its first coordination sphere. There are exceptions since, for example D1Asp170 also acts as a high affinity site for Mn2+ binding (38) so that the photo-oxidation of P680 to P680+ can facilitate its conversion to Mn3+ . In this way, as long as CaCl2 is present, the Mn4CaO5 is assembled step-by-step to form the OEC, a process known as photoactivation ( 39). 3. Chemical synthesis of OEC mimics. The very recent chemical synthesis of the Mn4CaO4 structure in organic solvent (25) shows that this cluster does not require protein to assemble and as long as there is an appropriate source of ligands, the structure is stable in an oxidised state. Moreover, cyclic voltammetery conducted in 1,2-dichloroethane showed that it can advance through the S-state cycle to S3 (25). However no oxygen evolution was detected when a small amount of water was present. Nevertheless, this extraordinary finding must have implications for the evolutionary origin of the OEC and provides some explanation for the robustness of the in vivo cluster to site directed mutations. Before the synthesis of the Mn4CaO4 cluster by Zhang et al, Christou and colleagues (40) reported the synthesis of a Mn3Ca2O4 molecule which is structurally similar to that of Mn4CaO4 (see 5C). Another important study was the synthesis of a Mn3CaO4 cubane by Agapie and colleagues (41b) (see Fig. 5D). However neither showed redox properties like that of the Mn4CaO4 synthesised by Zhang et al(25).


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Figure 5 Diagramatic comparison of synthesised cubane structures (B),(C) & (D) (refs 25, 40 & 41 respectively) with the Ferreira et al X-ray model(8) (A) and (E) a DFT calculated model of Siegbahn compared with the Umena el al X-ray structure (11) taken from ref. 13. For (A) to (D) Mn purple, Ca2+ green and red are oxo bonds. For (E) Ca is purple and Mn and O in pink distinguished by their size difference.

(4) Natural Mn oxide minerals The evolutionary origin of metal clusters in the catalytic center of metallo-enzymes is obscure. However in the case of the cubic Fe4S4-cluster of ferredoxins and other iron-sulphur proteins involved in electron transfer, it seems that this cubic geometry might have been derived from an iron sulphide mineral like greigite (42,43). The question is, could the Mn4CaO5-cluster of PSII originate from a naturally occurring MnO containing mineral? Just like the Fe4S4 cube it can, as detailed above, assemble in the absence of protein showing that it can be a purely independent inorganic molecule, at least as the Mn4CaO4 form.

Figure 6 (A) [Mn13Ca2O10(OH)2(OMe)2(O2CPh)18(H2O)4] macromolecule synthesised by Misra et al (48) composed of two building blocks shown in (B) and (C). Figure taken from ref.46. Ca is turquoise, Mn purple and yellow, and oxygen in red.

Manganese is a very abundant metal, second to iron. There are more than 30 Mn oxide/hydroxide minerals, and many of them occur in a wide variety of geological settings, particularly as nodules in ACS Paragon Plus Environment

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ocean beds(44). The Mn-O minerals, pyrolusite, ramsdellite, hollandite and romanechite have open lattices which bind cations like Ca2+. Indeed oxygen evolution from water splitting was observed using a number of Mn compounds (45,46) including mixing hollandite with an aqueous solution of the oxidising agent, cerium (IV) ammonium nitrate (47). That a Mn4CaO4 structure like that proposed by Ferreira et al can exist in the lattice of a macromolecular Mn-Ca molecule was shown by Misra et al (48). They synthesised a {Mn13Ca2O10(OH)2(OMe)2(O2CPh)18(H2O)4] molecule in a highly oxidised state (Fig. 6A) which consisted of two Mn4Ca building blocks. As can be seen in Fig 6, one form is the well known Mn4O4 cube (49) with a Ca attached to the cube by one of its bridging oxos (Fig. 6C) while the other building block (Fig. 6B) has a similar cubane structure to that of Mn4CaO4 of PSII. This study was the first to show that Mn and Ca can form discrete molecular complexes and also gave credibility to the Mn4CaO4 cubane model of Ferreira et al (8) before the 1.9 Å structure of Umena et al (11). Conclusions. (i) The cubane structure first proposed by Ferreira et al in 2004 and confirmed by Umena et al in 2011, is thermodynamically stable as long as appropriate ligands are available and remains in a oxidised state (Mn3+ and Mn4+). (ii) Its self assembly into PSII , in the presence of Ca2+, is powered by P680+ whereby Mn2+ is oxidized to higher valence states (eg Mn3+ and Mn4+) involving a high affinity binding site (D1Asp170). (iii) Many of the seven highly conserved amino acids coordinating the metal ions in vivo are replaceable and usually reduce the rate of oxygen evolution but often do not inhibit it completely so that the chemistry of O-O bond formation persists. Thus it seems that many of the ligands and other highly conserved amino acids in PSII act to optimize the rate of water oxidation including the efficient delivery of reactant (H2O) and removal of products (electrons (e), dioxygen (O2), protons(H+) ). Indeed, extensive H-bonding networks exist in the vicinity of the metal cluster and specific channels have been identified (11,50,51). This optimization also includes the requirement of two chloride molecules with one bound close to the mouth of a H+ channel (52). (iv) Although not yet shown, it seems reasonable to assume that the synthesised Mn4CaO4 cubane of Zhang et al (25) could evolve O2 at a low rate under oxidising conditions (Liao and Siegbahn personal communication) given that many different natural and synthetic CaMn compounds show some oxygen evolving activity. (45-47). However to get high rates of catalytic activity may need a “smart matrix” like that which has evolved for the OEC of PSII. (v) The predicted effect of significant radiation damage of the Mn4Ca2+-cluster during the collection of X-ray diffraction data (9,53 ) has turned out not to be the case and if there is an effect , it is very minor as shown by the very impressive femtosecond X-ray free-electron laser studies of Suga et al (14). Again this finding is consistent with the robustness of this metal oxide cluster. .

Acknowledgements. I would like to sincerely thank Dr James Murray for the preparation of Figures 2 and 5. References. 1. Debus, R. J. (1992) The manganese and calcium-ions of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1102, 269-352. 2. Barber, J. (2009) Photosynthetic energy conversion: natural and artificial. Chem. Soc. Revs. 38, 185-196. ACS Paragon Plus Environment

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3. Kok, B., Forbush, B., McGloin, M. (1970) Cooperation of charges in photosynthetic O2 evolution: A linear four step mechanism. Photochem. Photobiol. 11, 457-475. 4. Joliot, P., Barbieri, G. and Chabaud, R., 1969. Un nouveau modele des centres photochimiques du systeme II. Photochemistry and Photobiology, 10, 309-329. 5. Yachandra, V.K.(2002) Structure of the Mn complex in Photosystem II: Insights from X-ray spectroscopy. Phil Trans Roy Soc Lond B 357, 1347-1358. 6. Britt, R.D., Campbell, K.A., Peloquin, J.M., Gilchrist, M.L., Aznar, C.P., Dicus, M.M., Robblee, J. Messinger, J. (2004) Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1655, 158-171. 7. Haddy, A. (2007) EPR spectroscopy of the manganese cluster of photosystem II. Photosynthesis research, 92, 357-368. 8. Ferreira, K.N., Iverson, T.N., Maghlaoui, K., Barber, J., Iwata, S. (2004) Architecture of the Photosynthetic Oxygen-Evolving Center. Science, 303, 1831–1838. 9. Yano, J., Kern, J., Sauer, K., Latimer, M.J., Pushkar,Y., Biesiadka, J., Loll, B., Saenger, W., Messinger, J., Zouni, A. Yachandra, V.K., (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science, 314, 821-825. 10. Sproviero, E.M., Gascon, J.A., MaEvoy, J.P., Brudvig, G.W., Batista, V.S. (2008) Quantum Mechanics/Molecular Mechanics Study of the Catalytic Cycle of Water Splitting in Photosystem II J. Am. Chem. Soc. 130, 3428–3442. 11. Umena, Y., Kawaikami, K., Shen, J.R., Kamiya, N. (2011) Crystal structure of oxygen evolving photosystem II at a resolution of 1.9 angstrom. Nature 473, 55-65. 12. Dau, H., Grundmeier, A., Loja, P., Haumann, M. (2008) On the structure of the manganese complex of photosystem II: Extended-range EXAFS data and specific atomic-resolution models for four S-states. Philos Trans R Soc Lond B. 363, 1237–1243. 13. Siegbahn, P.E.M.. (2008) A structure-consistent mechanism for dioxygen formation in photosystem II. Chemistry 14, 8290–8302. 14. Suga, M., Akita, F., Hirata, K., Ueno, G., Murakami, H., Nakajima, Y., Shimizu, T., Yamashita, K., Yamamoto, M., Ago, H., Shen, J.R. (2015) Native structure of photosystem II at 1.95 A resolution viewed by femtosecond X-ray pulses. Nature 517, 99-103. 15. Luber, S., Rivalta, I., Umena, Y., Kawakami, K., Shen, J.R., Kamiya, N., Brudvig, G.W.,Batista, V.S. (2011) S1-state model of the O2-evolving complex of photosystem II. Biochemistry, 50, 6308-6311. 16. Yamanaka, S., Isobe, H., Kanda, K., Saito, T., Umena, Y., Kawakami, K., Shen, J.R., Kamiya, N., Okumura, M., Nakamura, H.,Yamaguchi, K. (2011) Possible mechanisms for the O–O bond


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53. Yano, J., Kern, J., Irrgang, K.D., Latimer, M.J., Bergmann, U., Glatzel, P., Pushkar, Y., Biesiadka, J., Loll, B., Sauer, K., Messinger, J. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proceedings of the National Academy of Sciences of the United States of America, 102, 12047-12052.


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For Table of Contents Use Only The Mn4Ca-cluster of the photosynthetic oxygen evolving center: its structure, function and evolution. James Barber


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Mn4Ca Cluster of Photosynthetic Oxygen-Evolving Center: Structure

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