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Photosynthetic water splitting by the Mn4Ca2+OX catalyst of photosystem II: its structure, robustness and mechanism

Published online by Cambridge University Press:  02 November 2017

James Barber
James Barber*
Affiliation:
Department of Life Sciences, Sir Ernst Chain Building, South Kensington Campus, Imperial College LondonSW7 2AZ, UK
*
*Author for correspondence: James Barber, Department of Life Sciences, Imperial College London, Sir Ernst Chain Building, South Kensington Campus, London SW7 2AZ, UK. Tel.: +44 208 747 1165; Fax: +44 207 594 5267; Email: j.barber@imperial.ac.uk
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Abstract

The biological energy cycle of our planet is driven by photosynthesis whereby sunlight is absorbed by chlorophyll and other accessory pigments. The excitation energy is then efficiently transferred to a reaction centre where charge separation occurs in a few picoseconds. In the case of photosystem II (PSII), the energy of the charge transfer state is used to split water into oxygen and reducing equivalents. This is accomplished by the relatively low energy content of four photons of visible light. PSII is a large multi-subunit membrane protein complex embedded in the lipid environment of the thylakoid membranes of plants, algae and cyanobacteria. Four high energy electrons, together with four protons (4H+), are used to reduce plastoquinone (PQ), the terminal electron acceptor of PSII, to plastoquinol (PQH2). PQH2 passes its reducing equivalents to an electron transfer chain which feeds into photosystem I (PSI) where they gain additional reducing potential from a second light reaction which is necessary to drive CO2 reduction. The catalytic centre of PSII consists of a cluster of four Mn ions and a Ca2+ linked by oxo bonds. In addition, there are seven amino acid ligands. In this Article, I discuss the structure of this metal cluster, its stability and the probability that an acid-base (nucleophilic-electrophilic) mechanism catalyses the water splitting reaction on the surface of the metal-cluster. Evidence for this mechanism is presented from studies on water splitting catalysts consisting of organo-complexes of ruthenium and manganese and also by comparison with the enzymology of carbon monoxide dehydrogenase (CODH). Finally the relevance of our understanding of PSII is discussed in terms of artificial photosynthesis with emphasis on inorganic water splitting catalysts as oxygen generating photoelectrodes.

Type
Review
Information
Quarterly Reviews of Biophysics , Volume 50 , 2017 , e13
Copyright
Copyright © Cambridge University Press 2017 

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References

Ames, W., Pantazis, D. A., Krewald, V., Cox, N., Messinger, J., Lubitz, W. & Neese, F. (2011). Theoretical evaluation of structural models of the S2 state in the oxygen evolving complex of photosystem II: protonation states and magnetic interactions. Journal of the American Chemical Society 133, 19743–19757.CrossRefGoogle Scholar
Ananyev, G. M. & Dismukes, G. C. (1996). Assembly of the tetra-Mn site of photosynthetic water oxidation by photoactivation: Mn stoichiometry and detection of a new intermediate. Biochemistry 35, 4102–4109.Google Scholar
Askerka, M., Wang, J., Vinyard, D. J., Brudvig, G. W. & Batista, V. S. (2016). S3 state of the O2-evolving complex of photosystem II: insights from QM/MM, EXAFS, and femtosecond X-ray diffraction. Biochemistry 55, 981–984.CrossRefGoogle ScholarPubMed
Barber, J. (2003). Photosystem II: the engine of life. Quarterly Reviews of Biophysics 36, 71–89.Google Scholar
Barber, J. (2009). Photosynthetic energy conversion: natural and artificial. Chemical Society Reviews 38, 185–196.CrossRefGoogle ScholarPubMed
Barber, J. (2016a). Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere. Quarterly Reviews of Biophysics 49, 1–21.Google Scholar
Barber, J. (2016b). Mn4Ca cluster of photosynthetic oxygen-evolving center: structure, function and evolution. Biochemistry 55, 5901–5906.CrossRefGoogle ScholarPubMed
Barber, J. (2017). A mechanism for water splitting and oxygen production in photosynthesis. Nature Plants 3, 17041–17046.CrossRefGoogle ScholarPubMed
Barber, J. & Andersson, B. (1992). Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Sciences 17, 61–66.CrossRefGoogle ScholarPubMed
Barber, J., Ferreira, K., Maghlaoui, K. & Iwata, S. (2004). Structural model of the oxygen-evolving centre of photosystem II with mechanistic implications. Physical Chemistry and Chemical Physics 6, 4737–4742.Google Scholar
Bassi, P. S., Wong, L. H. & Barber, J. (2014). Iron based photoanodes for solar fuel production. Physical Chemistry and Chemical Physics 16, 11834–11842.Google Scholar
Boussac, A., Rutherford, A. W. & Styring, S. (1990). Interaction of ammonia with the water splitting enzyme of photosystem II. Biochemistry 29, 24–32.Google Scholar
Bovi, D., Narzi, D. & Guidoni, L. (2013). The S2 state of the oxygen? Evolving complex of photosystem II explored by QM/MM dynamics: spin surfaces and metastable states suggest a reaction path towards the S3 state. Angewandte Chemie – International Edition 52, 11744–11749.Google Scholar
Britt, R. D., Campbell, K. A., Peloquin, J. M., Gilchrist, M. L., Aznar, C. P., Cicus, M. M., Robble, 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 1655, 158–171.CrossRefGoogle ScholarPubMed
Brudvig, G. W. (2008). Water oxidation chemistry of photosystem II. Philosophical Transaction of the Royal Society of London B 363, 1211–1218.Google Scholar
Buchel, C., Barber, J., Ananyev, G., Eshaghi, S., Watts, R. & Dismukes, C. (1999). Photoassembly of the manganese cluster and oxygen evolution from monomeric and dimeric CP47-reaction centre photosystem II complexes. Proceedings of the National Academy of Sciences of the United States of America, 96, 14288–14293.CrossRefGoogle ScholarPubMed
Cady, C. W., Crabtree, R. H. & Brudvig, G. W. (2008). Functional models for the oxygen-evolving complex of photosystem II. Coordination Chemistry Reviews 252, 444–455.Google Scholar
Clausen, J., Winkler, S., Hays, A. M. A., Hundelt, M., Debus, R. J. & Junge, W. (2001). Photosynthetic water oxidation in Synechocystis sp. PCC6803: mutations D1-E189K, R and Q are without influence on electron transfer at the donor side of photosystem II. Biochimica et Biophysica Acta 1506, 224–235.Google Scholar
Concepcian, J. J., Jurss, J. W., Brennaman, M. K., Hoertz, P. G., Patrocinio, A. O. T., Murakami Iha, N. T., Templeton, J. L. & Meyer, T. J. (2009). Making oxygen with ruthenium complexes. Accounts of Chemical Research 42, 1954–1965.CrossRefGoogle Scholar
Cox, N., Retegan, M., Neese, F., Pantais, D. A., Boussac, A. & Lubitz, W. (2014). Electronic structure of the oxygen-evolving complex in photosystem II prior to O–O bond formation. Science 345, 804–808.CrossRefGoogle ScholarPubMed
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. Philosophical Transaction of the Royal Society of London B 363, 1237–1243.Google Scholar
Dau, H. & Haumann, M. (2007). Eight steps preceding O–O bond formation in oxygenic photosynthesis-a basic reaction cycle of the photosystem II manganese complex. Biochimica et Biophysica Acta 1767, 472–483.Google Scholar
Debus, R. J. (1992). The manganese and calcium-ions of photosynthetic oxygen evolution. Biochimica et Biophysica Acta 1102, 269–352.Google Scholar
Debus, R. J. (2008). Protein ligation of the photosynthetic oxygen-evolving center. Coordination Chemistry Reviews 252, 244–258.CrossRefGoogle ScholarPubMed
De Saussure, N.-T. (1804). Reserches Chimique sur la Vegetation. Nyon, Paris: Annales de chimie (‘Annals of Chemistry’).Google Scholar
Diner, B. A., Nixon, P. J. & Farchaus, J. W. (1991). Site-directed mutagenesis of photosynthetic reaction centers. Current Opinion in Structural Biology 1, 546–554.Google Scholar
Dobbek, H., Svetlitchnyi, V., Gremer, L., Huber, R. & Meyer, O. (2001). Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293, 1281–1285.Google Scholar
Du, P. & Eisenberg, R. (2012). Catalysts made of earth-abundant elements (Co, Ni, Fe) for water splitting: recent progress and future challenges. Energy and Environmental Science 5, 6012–6021.Google Scholar
Duan, L., Bozoglian, F., Mandal, S., Stewart, B., Privalov, T., Llobet, A. & Sun, L. (2012). A molecular ruthenium catalyst with water-oxidation activity comparable to that of photosystem II. Nature Chemistry 4, 418–423.CrossRefGoogle ScholarPubMed
Duan, L., Wang, L., Li, F., Li, F., Sun, L. (2015). Highly efficient bioinspired molecular Ru water oxidation catalysts with negatively charged backbone ligands. Accounts of Chemical Research 48, 2084–2096.CrossRefGoogle ScholarPubMed
Eisenberg, R. & Gray, H. B. (2008). Preface on making oxygen. Inorganic Chemistry 47, 1697–1699.Google Scholar
Ferreira, K., Iverson, T. M., Maglaoui, K., Barber, J. & Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838.Google Scholar
Fesseler, J., Jeoung, J-H. & Dobbek, H. (2015). How the [NiFe4S4] cluster of CO dehydrogenase activates CO2 and NCO. Angewandte Chemie – International Edition 54, 8560–8564.Google Scholar
Fontana, F. (1780). Accounts of air extracted from different kinds of water. Philosophical Transactions of the Royal Society of London B 69, 432–453.Google Scholar
Gao, Y., Åkermark, T., Liu, J., Sun, L. & Åkermark, B. (2009). Nucleophilic attack of hydroxide on a MnV-oxo complex: a model of the O–O bond formation in the oxygen evolving complex of photosystem II. Journal of American Chemical Society 131, 8726–8727.Google Scholar
Gao, Y., Liu, J., Wang, M., Na, Y., Åkermark, B. & Sun, L. (2007). Synthesis and characterization of manganese and copper corrole xanthene complexes as catalysts for water oxidation. Tetrahedron 63, 1987–1994.Google Scholar
Gersten, S. W., Samuels, G. J. & Meyer, T. J. (1982). Catalytic oxidation of water by an oxo-bridged ruthenium dimer. Journal of American Chemical Society 104, 4029–4030.CrossRefGoogle Scholar
Gong, W. M., Hao, B., Wei, Z., Ferguson, D. J. Jr., Tallant, T., Krzycki, J. A. & Chan, M. K. (2008). Structure of the α2ε2 Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase/synthase complex. Proceedings of the National Academy of Sciences of the United States of America 105, 9558–9563.CrossRefGoogle ScholarPubMed
Gurudayal, Sabba, D., Kumar, M. H., Wong, L. H., Barber, J., Graetzel, M. & Mathews, N. (2015). Perovskite-hematite tandem cells for efficient overall solar driven water splitting. Nano Letters 15, 3833–3839.Google Scholar
Gurudayal, , Chaim, S. Y., Kumar, M. H., Bassi, P. S., Seng, H. L., Barber, J. & Wong, L. H. (2014). Improving the efficiency of hematite nanorods for photoelectrochemical water splitting by doping with manganese. ACS Applied Materials & Interfaces 6, 5852–5859.Google Scholar
Haddy, A. (2007). EPR spectroscopy of the manganese cluster of photosystem II. Photosynthesis Research 92, 357–368.Google Scholar
Haumann, M., Liebisch, P., Muller, C., Barra, M., Grabolle, M. & Dau, H. (2005). Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310, 1019–1021.CrossRefGoogle ScholarPubMed
Hill, R. (1937). Oxygen evolution by isolated chloroplasts. Nature 139, 881–882.CrossRefGoogle Scholar
Hill, R. (1972). Foreward. In Proceedings of the 2nd International Congress on Photosynthesis Research, vol. 1 (eds. Forti, G., Avron, M. & Melandri, B. A.), pp. 1–18. The Hague: Junk.Google Scholar
Hoganson, C. W. & Babcock, G. T. (1997). A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277, 1953–1956.Google Scholar
Jeoung, J. H. & Dobbek, H. (2007). Carbon dioxide activation at the Ni, Fe-cluster of anaerobic carbon monoxide dehydrogenase. Science 318, 1461–1464.Google Scholar
Jiao, F. & Frei, H. (2010). Nanostructured manganese oxide clusters supported on mesoporous silica as efficient oxgen-evolving catalysts. Chemical Communications 46, 2920–2922.Google Scholar
Joliot, P., Barbieri, G. & Chabaud, R. (1969). Un nouveau modele des centres photochimiques du systeme II. Photochemistry and Photobiology 10, 309–329.CrossRefGoogle Scholar
Kanady, S., Tsui, E., Day, M. & Agapie, T. (2011). A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333, 733–736.CrossRefGoogle ScholarPubMed
Kanan, M. W. & Nocera, D. G. (2008). In situ formation of an oxygen-evolving catalyst in neutral water containing phosphate and Co2+ . Science 321, 1072–1075.Google Scholar
Kok, B., Forbush, B. & McGLOIN, M. (1970). Cooperation of charges in photosynthetic O2 evolution. 1. A linear four-step mechanism. Photochemistry and Photobiology 11, 467–475.CrossRefGoogle Scholar
Le Formal, F., Pastor, E., Tilley, S. D., Mesa, C. A., Pendlebury, R., Graetzel, M. & Durrant, J. R. (2015). Rate law analysis of water oxidation on a Hematie surface. Journal of the American Chemical Society 137, 6629–6637.Google Scholar
Li, X. and Siegbahn, P. E. (2015). Alternative mechanisms for O2 release and O–O bond formation in the oxygen evolving complex of photosystem II. Physical Chemistry Chemical Physics 17, 12168–12174.Google Scholar
Limburg, J., Brudvig, G. W. & Crabtree, R. H. (1997). O2 evolution and permanganate formation from high-valent manganese complexes. Journal of American Chemical Society 119, 2761–2762.Google Scholar
Limburg, J., Vrettos, J. S., Liable-Sands, L. M., Rheingold, A. L., Crabtree, R. H. & Brudvig, G. W. (1999). A functional model for O–O bond formation by the O2-evolving complex in photosystem II. Science 283, 1524–1527.Google Scholar
Limburg, J., Vrettos, J. S., Chen, H., De Paula, J. C., Crabtree, R. H. & Brudvig, G. W. (2001). Characterization of the O2-evolving reaction catalyzed by [(terpy)(H2O) MnIII (O) 2MnIV (OH2)(terpy)](NO3) 3 (terpy = 2,2′:6,2″-terpyridine). Journal of American Chemical Society 123, 423–430.Google Scholar
Liu, F., Concepcion, J. J., Jurss, J. W., Cardolaccia, T., Templeton, J. L. & Meyer, T. J. (2008). Mechanisms of water oxidation from the blue dimer to photosystem II. Inorganic Chemistry, 47, 1727–1752.Google Scholar
Lohmiller, T., Krewald, V., Navarro, M. P., Retegan, M., Rapatskiy, L., Nowaczyk, M. M., Boussac, A., Neese, F., Lubitz, W., Pantazis, D. A. & Cox, N. (2014). Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study. Physical Chemistry Chemical Physics 16, 11877–11892.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Matheu, R., Ertem, M. Z., Benet-Buchholz, J., Coronado, E., Batista, V. S., Sala, X. & Llobet, A. (2015). Intramolecular proton transfer boosts water oxidation catalyzed by a Ru complex. Journal of American Chemical Society 137, 10786–10795.Google Scholar
McConnell, I. L., Grigoryants, V. M., Scholes, C. P., Myers, W. K., Chen, P. Y., Whittaker, J. W. & Brudvig, G. (2012). EPR-ENDOR characterization of (17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II. Journal of American Chemical Society 134, 1504–1512.Google Scholar
Merki, D. & Hu, X. (2011). Recent developments of molybdenum and tungsten as hydrogen evolution catalysts. Energy and Environmental Science, 4, 3878–3888.Google Scholar
Messinger, J., Badger, M. & Wydrzynski, T. (1995). Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proceedings of the National Academy of Sciences of the United States of America 92, 3209–3213.CrossRefGoogle ScholarPubMed
Misra, A., Wernsdorfer, W., Abboud, K. A. & Christou, G. (2005). The first high oxidation state manganese-calcium cluster: relevance to the water oxidizing complex of photosynthesis. Chemical Communications 1, 54–56.CrossRefGoogle Scholar
Mukherjee, S., Stull, J. A., Yano, J., Stamatato, T., Pringouri, K., Stich, T. A., Abbroud, K. A., Britt, R. D., Yachandra, V. K. & Christou, G. (2012). Synthetic model of the asymmetric [Mn3CaO4] cubane core of the oxygen-evolving complex of photosystem II. Proceedings of the National Academy of Sciences of the United States of America 109, 2257–2262.Google Scholar
Murakami, M., Hong, D., Suenobu, T., Yamaguchi, S., Ogura, T. & Fukuzumi, S. (2011). Catalytic mechanism of water oxidation with single-site ruthenium-heteropolytungstate complexes. Journal of American Chemical Society 133, 11605–11613.Google Scholar
Murphy, A. B., Barnes, P. R. F., Randeniy, L. K., Plumb, I. C., Grey, I. E., Horne, M. D. & Glasscock, J. A. (2006). Efficiency of solar water splitting using semiconductor electrodes. International Journal of Hydrogen Energy 31, 1999–2017.Google Scholar
Murray, J. W. (2012). Sequence variation at the oxygen-evolving centre of photosystem II: a new class of ‘rogue'cyanobacterial D1 proteins. Photosynthesis Research 110, 177–184.Google Scholar
Murray, J. W. & Barber, J. (2007). Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. Journal of Structural Biology 159, 228–237.Google Scholar
Najafpour, M. M. (2011). Hollandite as a functional and structural model for the biological water oxidizing complex: manganese-calcium oxide minerals as a possible evolutionary origin for the CaMn4 cluster of the biological water oxidizing complex. Geomicrobiology Journal, 28, 714–718.Google Scholar
Najafpour, M. M., Ehrenberg, T., Wiechen, M. & Kurz, P. (2010). Calcium manganese (III) oxides (CaMn2O4×H2O) as biomimetic oxygen-evolving catalysts. Angewandte Chemie – International Edition 49, 2233–2237.Google Scholar
Najafpour, M. M., Rahimi, F., Aro, E. M., Lee, C. H. & Allakhverdiev, S. I. (2012). Nano-sized manganese oxides as biomimetic catalysts for water oxidation in artificial photosynthesis: a review. Journal of the Royal Society Interface 9, 2383–2395.Google Scholar
Navarro, M. P., Ames, W. M., Nilsson, H., Lohmiller, T., Pantazis, D. A., Rapatskiy, L., Nowaczyk, M. M., Neese, F., Boussac, A., Messinger, J. & Lubitz, W. (2013). Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer. Proceedings of the National Academy of Sciences of the United States of America 110, 15561–15566.Google Scholar
Oyala, P. H., Stich, T. A., Debus, R. J. & Britt, R. D. (2015). Ammonia binds to the dangler manganese of the photosystem II oxygen-evolving complex. Journal of the American Chemical Society 137, 8829–8837.Google Scholar
Pecararo, V. L., Baldwin, M. J., Caudl, M. T., Hsieh, W. Y. & Law, N. A. (1998). A proposal for water oxidation in photosystem II. Pure and Applied Chemistry 70, 925–929.CrossRefGoogle Scholar
Pecararo, V. L., Baldwin, M. J. & Gelasco, A. (1994). Interaction of manganese with dioxygen and its reduced derivatives. Chemical Reviews 94, 807–826.CrossRefGoogle Scholar
Peloquin, J. M. & Britt, R. D. (2001). EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1503, 96–111.Google Scholar
Perez-Navarro, M., Neese, F., Lubitz, W., Pantazis, D. A. & Cox, N. (2016). Recent developments in biological water oxidation. Current Opinion in Chemical Biology 31, 113–119.Google Scholar
Preistley, J. (1772). Observations on different kinds of air. Philosophical Transactions of the Royal Society of London B 62, 147–264.Google Scholar
Rabinowitch, E. (1945). Photosynthesis and Related Processes, vol. 1. New York: Intersciences.Google Scholar
Rapatskiy, L., Cox, N., Savitsky, A., Ames, W. M., Sander, J., Nowaczyk, M. M., Rogner, M., Boussac, A., Neese, F., Messinger, J. & Lubitz, W. (2012). Detection of the water-binding sites of the oxygen-evolving complex of photosystem II using W-band 17O electron-electron double resonance-detected NMR spectroscopy. Journal of American Chemical Society 134, 16619–16634.Google Scholar
Reece, S. Y., Hamel, J. A., Sung, K., Jarvi, T. D., Esswein, A. J., Pijpers, J. J. & Nocera, D. G. (2011). Wireless solar water splitting using silicon-based semiconductors and earth-abundant catalysts. Science 334, 645–648.Google Scholar
Risch, M., Khare, V., Zaharieva, I., Gerencser, L., Cherney, P. & Dau, H. (2009). Cobalt-oxo core of a water-oxidizing catalyst film. Journal of American Chemical Society 131, 6936–6937.Google Scholar
Ruben, S., Randle, M., Kaman, M. & Hyde, J. L. (1941). Heavy oxygen (O18) as a tracer in the study of photosynthesis. Journal of American Chemical Society 63, 877–879.Google Scholar
Ruettinger, W. F., Ho, D. M. & Dismukes, G. C. (1999). Protonation and dehydration reactions of the Mn4O4L6 cubane and synthesis and crystal structure of the oxidized cubane [Mn4O4L6]+: a model for the photosynthetic water oxidizing complex. Inorganic Chemistry 38, 1036–1037.Google Scholar
Sala, X., Maji, S., Bofill, R., Garcia-Anton, J., Escriche, L. & Llobet, A. (2013). Molecular water oxidation mechanisms followed by transition metals: state of the art. Accounts of Chemical Research 47, 504–516.Google Scholar
Service, R. J., Yano, J., McCONNELL, I., Hwang, H. J., Niks, D., Hille, R., Wydrzynski, T., Burnap, R. L., Hillier, W. & Debus, R. J. (2010). Participation of glutamate-354 of the CP43 polypeptide in the ligation of manganese and the binding of substrate water in photosystem II. Biochemistry 50, 63–81.Google Scholar
Siegbahn, P. E. M. (2006). O–O bond formation in the S4-state of the oxygen evolving complex in photosystem II. Chemistry – A European Journal 12, 9217–9237.Google Scholar
Siegbahn, P. E. M. (2008). A structure-consistent mechanism for dioxygen formation in photosystem II. Chemistry – A European Journal 14, 8290–8302.Google Scholar
Siegbahn, P. E. M. (2009). Structures and energetics for O2 formation in photosystem II. Accounts of Chemical Research 42, 1871–1880.Google Scholar
Siegbahn, P. E. M. (2013). Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O–O bond formation and O2 release. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1827, 1003–1019.Google Scholar
Siegbahn, P. E. M. & Crabtree, R. H. (1999). Manganese oxyl radical intermediates and OO bond formation in photosynthetic oxygen evolution and a proposed role for the calcium cofactor in photosystem II. Journal of American Chemical Society 121, 117–127.Google Scholar
Sivula, K., Le Formal, F. & Graetzel, M. (2011). Solar water splitting: progress using hematite (αFe2O3) photoelectrodes. ChemSusChem 4, 432–449.CrossRefGoogle ScholarPubMed
Smith, R. J., Loganathan, M. & Shantha, M. S. (2010). A review of the water gas shift reaction kinetics. International Journal of Chemical Reactor Engineering 8, 1–32.Google Scholar
Sproviero, E. M., Gascon, J. A., McEVOY, J. P., Brudvig, G. W. & Batista, V. (2008). Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. Journal of American Chemical Society 130, 3428–3442.Google Scholar
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.CrossRefGoogle ScholarPubMed
Suga, M., Akita, F., Sugahara, M., Kubo, M., Nakajima, Y., Nakane, T., Yamashita, K., Umena, Y., Nakabayashi, M., Yamane, T., Nakano, T., Suzuki, M., Masuda, T., Inoue, S., Kimura, T., Nomura, T., Yonekura, S., Yu, L.-J., Sakamoto, T., Motomura, T., Chen, J.-H., Kato, Y., Noguchi, T., Tono, K., Joti, Y., Kameshima, T., Hatsui, T., Nango, E., Tanaka, R., Naitow, H., Matsuura, Y., Yamashita, A., Yamamoto, M., Nureki, O., Yabashi, M., Ishikawa, T., Iwata, S. & Shen, J.-R. (2017). Light-induced structural changes and the site of O–O bond formation in PSII caught by XFEL. Nature 543, 131–135.Google Scholar
Svetlitchnyi, V., Dobbek, H., Meyer-Klaucke, W., Meins, T., Thiele, B., Romer, P., Huber, R. & Meyer, O. (2004). A functional Ni-Ni-[4Fe-4S] cluster in the monomeric acetyl-CoA synthase from carboxydothermus hydrogenoformans. Proceedings of the National Academy of Sciences of the United States of America 101, 446–451.Google Scholar
Tagore, R., Crabtree, R. H. & Brudvig, G. W. (2008). Oxygen evolution catalysis by a dimanganese complex and its relation to photosynthetic water oxidation. Inorganic Chemistry 47, 1815–1823.Google Scholar
Tommas, C. & Babcock, G. T. (1998). Oxygen production in nature: a light-driven metalloradical enzyme process. Accounts of Chemical Research 31, 18–25.Google Scholar
Tong, L., Duan, L., Xu, Y., Privalov, T. & Sun, L. (2011). Structural modifications of mononuclear ruthenium complexes: a combined experimental and theoretical study on the kinetics of ruthenium catalyzed water oxidation. Angewandte Chemie – International Edition 50, 445–449.Google Scholar
Tran, P. D., Artero, V. & Fontecave, M. (2010). Water electrolysis and photoelectrolysis on electrodes engineered using biological and bio-inspired molecular systems. Energy and Environmental Science 3, 727–747.Google Scholar
Tran, P. D. & Barber, J. (2012). Proton reduction to hydrogen in biological and chemical systems. Physical Chemistry Chemical Physics 14, 13772–13784.Google Scholar
Tran, P. D., Chaim, S. Y., Boix, P. P., Ren, Y., Pramana, S. S., Fize, J., Artero, V. & Barber, J. (2013). Novel cobalt/nickel-tungsten-sulfide catalysts for electrocatalytic hydrogen generation from water. Energy and Environmental Science 6, 2452–2459.Google Scholar
Tran, P. D., Tran, T. V., Orio, M., Torelli, S., Truon, Q. D., Nayuki, K., Sasaki, Y., Chiam, S. Y., Yi, R., Honma, I., Barber, J. & Artero, V. (2016). Coordination polymer structure and revisited hydrogen evolution catalytic mechanism for amorphous molybdenum sulfide. Nature Materials 15, 640–646.Google Scholar
Tran, P. D., Wong, L. H., Barber, J. & Loo, J. S. (2012). Recent advances in hybrid photocatalysts for solar fuel production. Energy and Environmental Science 5, 5902–5918.Google Scholar
Umena, Y., Kawakami, K., Shen, J. R. & Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1·9 Å. Nature 473, 55–60.Google Scholar
Van Ingen-Housz, J. (1779). Experiments upon Vegetables, Experiments upon vegetables discovering their great power of purifying the common air in the sun-shine, and of injuring it in the shade and at night: to which is joined, a new method of examining the accurate degree of salubrity of the atmosphere. Pub. P. Elmsly and H. Payne, London.Google Scholar
Van Neil, C. B. (1941). The bacterial photosyntheses and their importance for the general problem of photosynthesis. Advances in Enzymology 1, 263–328.Google Scholar
Vinyard, D. J. & Brudvig, G. W. (2017) Progress toward a molecular mechanism of water oxidation in photosystem II. Annual Review of Physical Chemistry 68. In press.Google Scholar
Vinyard, D. J., Khan, S. & Brudvig, G. W. (2015) Photosynthetic water oxidation: binding and activation of substrate waters for O–O bond formation. Faraday Discussions 185, 37–50.Google Scholar
Vrettos, J. S., Limberg, J. & Brudvig, G. W. (2001). Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochimica et Biophysica Acta 1503, 229–245.Google Scholar
Wang, M., Chen, L. & Sun, L. (2012). Recent progress in electrochemical hydrogen production with earth-abundant metal complexes as catalysts. Energy & Environmental Science 5, 6763–6778.Google Scholar
Yachandra, V. K. (2002). Structure of the Mn complex in photosystem II: insights from X-ray spectroscopy. Philosophical Transaction of the Royal Society of London B 357, 1347–1358.Google Scholar
Yamanaka, S., Isobe, H., Kanda, K., Saito, T., Umena, Y., Kawakami, K., Shen, J. R., Kamiya, N., Okumur, M., Nakamura, H. & Yamaguchi, K. (2011). Possible mechanisms for the O–O bond formation in oxygen evolution reaction at the CaMn4O5(H2O)4 cluster of PSII refined to 1·9 Å X-ray resolution. Chemical Physics Letters 511, 138–145.Google Scholar
Yano, J., Kern, J., Irrgang, K. D., Latimar, M. J., Bergmann, U., Glatzel, P., Pushkar, Y. J., Loll, B., Sauer, K., Messinger, J. & Yachandra, V. K. (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.Google Scholar
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 3, 821–825.Google Scholar
Young, I. D., Ibrahim, M., Chatterjee, R., Gul, S., Fuller, F., Koroidov, S., Brewster, A. S., Tran, R., Alonso-Mori, R., Kroll, T., Michels-Clark, T., Laksmono, H., Sierra, R. G., Stan, C. A., Hussein, R., Zhang, M., Douthit, L., Kubin, M., de Lichtenberg, C., Long Vo, P., Nilsson, H., Cheah, M. H., Shevela, D., Saracini, C., Bean, M. A., Seuffert, I., Sokaras, D., Weng, T.-C., Pastor, E., Weninger, C., Fransson, T., Lassalle, L., Bräuer, P., Aller, P., Docker, P. T., Andi, B., Orville, A. M., Glownia, J. M., Nelson, S., Sikorski, M., Zhu, D., Hunter, M. S., Lane, T. J., Aquila, A., Koglin, J. E., Robinson, J., Liang, M., Boutet, S., Lyubimov, A. Y., Uervirojnangkoorn, M., Moriarty, N. W., Liebschner, D., Afonine, P. V., Waterman, D. G., Evans, G., Wernet, P., Dobbek, H., Weis, W. I., Brunger, A. T., Zwart, P. H., Adams, P. D., Zouni, A., Messinger, J., Bergmann, U., Sauter, N. K., Kern, J., Yachandra, V. K. & Yano, J. (2016). Structure of photosystem II and substrate binding at room temperature. Nature 540, 453–457.Google Scholar
Zaharieva, I., Najafpour, M. M., Wiechert, M., Haumann, M., Kurz, P. & Dau, H. (2011). Synthetic manganese–calcium oxides mimic the water-oxidizing complex of photosynthesis functionally and structurally. Energy and Environmental Science 4, 2400–2408.Google Scholar
Zhang, C., Chen, C., Dong, H., Shen, J. R., Dau, H. & Zhao, J. (2015). A synthetic Mn4Ca-clustermimicking the oxygen-evolving center of photosynthesis. Science 348, 690–693.Google Scholar
Zong, X., Han, J., Ma, G., Yan, H., Wu, G. & Li, C. (2011). Photocatalytic H2 evolution on CdS loaded with WS2 as co-catalyst under visible light irradiation. The Journal of Physical Chemistry 115, 12202–12208.Google Scholar