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Oxygenic photosynthesis: history, status and perspective

Published online by Cambridge University Press:  23 January 2019

Wolfgang Junge
Wolfgang Junge*
Affiliation:
Universität Osnabrück, 49069 Osnabrück, Germany
*
Author for correspondence: Wolfgang Junge, E-mail: junge@uos.de
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Abstract

Cyanobacteria and plants carry out oxygenic photosynthesis. They use water to generate the atmospheric oxygen we breathe and carbon dioxide to produce the biomass serving as food, feed, fibre and fuel. This paper scans the emergence of structural and mechanistic understanding of oxygen evolution over the past 50 years. It reviews speculative concepts and the stepped insight provided by novel experimental and theoretical techniques. Driven by sunlight photosystem II oxidizes the catalyst of water oxidation, a hetero-metallic Mn4CaO5(H2O)4 cluster. Mn3Ca are arranged in cubanoid and one Mn dangles out. By accumulation of four oxidizing equivalents before initiating dioxygen formation it matches the four-electron chemistry from water to dioxygen to the one-electron chemistry of the photo-sensitizer. Potentially harmful intermediates are thereby occluded in space and time. Kinetic signatures of the catalytic cluster and its partners in the photo-reaction centre have been resolved, in the frequency domain ranging from acoustic waves via infra-red to X-ray radiation, and in the time domain from nano- to milli-seconds. X-ray structures to a resolution of 1.9 Å are available. Even time resolved X-ray structures have been obtained by clocking the reaction cycle by flashes of light and diffraction with femtosecond X-ray pulses. The terminal reaction cascade from two molecules of water to dioxygen involves the transfer of four electrons, two protons, one dioxygen and one water. A rigorous mechanistic analysis is challenging because of the kinetic enslaving at millisecond duration of six partial reactions (4e−, 1H+, 1O2). For the time being a peroxide-intermediate in the reaction cascade to dioxygen has been in focus, both experimentally and by quantum chemistry. Homo sapiens has relied on burning the products of oxygenic photosynthesis, recent and fossil. Mankind's total energy consumption amounts to almost one-fourth of the global photosynthetic productivity. If the average power consumption equalled one of those nations with the highest consumption per capita it was four times greater and matched the total productivity. It is obvious that biomass should be harvested for food, feed, fibre and platform chemicals rather than for fuel.

Keywords

Photosynthesiswater oxidationoxygenmanganese cluster
Type
Review
Information
Quarterly Reviews of Biophysics , Volume 52 , 2019 , e1
Copyright
Copyright © Cambridge University Press 2019 

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References

Ahlbrink, R, Haumann, M, Cherepanov, D, Bogershausen, O, Mulkidjanian, A and Junge, W (1998) Function of tyrosine Z in water oxidation by photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry 37, 1131–1142.Google Scholar
Ahrling, KA and Pace, RJ (1995) Simulation of the S2 state multiline electron paramagnetic resonance signal of photosystem II: a multifrequency approach. Biophysical Journal 68, 2081–2090.Google Scholar
Akerlund, HE, Andersson, B and Albertsson, PA (1976) Isolation of photosystem-ii enriched membrane-vesicles from spinach-chloroplasts by phase partition. Biochimica et Biophysica Acta 449, 525–535.Google Scholar
Amin, M, Badawi, A and Obayya, SS (2016) Radiation damage in XFEL: case study from the oxygen-evolving complex of photosystem II. Scientific Reports 6:36492, 1–6.Google Scholar
Amin, M, Askerka, M, Batista, VS, Brudvig, GW and Gunner, MR (2017) X-ray free electron laser radiation damage through the s-state cycle of the oxygen-evolving complex of photosystem II. Journal of Physical Chemistry B 121, 9382–9388.Google Scholar
Anderson, JM and Andersson, B (1988) The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends in Biochemical Sciences 13, 351–355.Google Scholar
Andersson, B (2005) Introduction to the special issue dedicated to James Barber. Photochemical & Photobiological Sciences 4, 930–931.Google Scholar
Andersson, B and Anderson, JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochimica et Biophysica Acta 593, 427–440.Google Scholar
Andersson, B, Akerlund, HE and Albertsson, PA (1977) Light-induced reversible proton extrusion by spinach-chloroplast photosystem 2 vesicles isolated by phase partition. FEBS Letters 77, 141–145.Google Scholar
Askerka, M, Brudvig, GW and Batista, VS (2017) The O-2-evolving complex of photosystem II: recent insights from Quantum Mechanics/Molecular Mechanics (QM/MM), Extended X-ray Absorption Fine Structure (EXAFS), and femtosecond X-ray crystallography data. Accounts of Chemical Research 50, 41–48.Google Scholar
Babcock, GT and Sauer, K (1973) Electron paramagnetic resonance signal II in spinach chloroplasts. I. Kinetic analysis for untreated chloroplasts. Biochimica et Biophysica Acta 325, 483–503.Google Scholar
Babcock, GT and Sauer, K (1975) Rapid component of electron-paramagnetic resonance signal II – candidate for physiological donor to photosystem-II in spinach-chloroplasts. Biochimica et Biophysica Acta 376, 329–344.Google Scholar
Bar-On, YM, Phillips, R and Milo, R (2018) The biomass distribution on Earth. Proceedings of the National Academy of Sciences of the United States of America 115, 6506–6511.Google Scholar
Barber, J (2016) Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere. Quarterly Reviews of Biophysics 49, 1–20.Google Scholar
Barber, J (2017) A mechanism for water splitting and oxygen production in photosynthesis. Nature Plants 3:17041, 1–5.Google Scholar
Barter, LMC, Bianchietti, M, Jeans, C, Schilstra, MJ, Hankamer, B, Diner, BA, Barber, J, Durrant, JR and Klug, DR (2001) Relationship between excitation energy transfer, trapping, and antenna size in photosystem II. Biochemistry 40, 4026–4034.Google Scholar
Bekker, A, Holland, HD, Wang, PL, Rumble, D, Stein, HJ, Hannah, JL, Coetzee, LL and Beukes, NJ (2004) Dating the rise of atmospheric oxygen. Nature 427, 117–120.Google Scholar
Berthold, DA, Babcock, GT and Yocum, CF (1981) A highly resolved, oxygen-evolving photosystem-ii preparation from spinach thylakoid membranes – electron-paramagnetic-res and electron-transport properties. FEBS Letters 134, 231–234.Google Scholar
Blankenship, RE (2014) Molecular Mechanisms of Photosynthesis. Chichester: Wiley Blackwell.Google Scholar
Blankenship, RE and Sauer, K (1974) Manganese in photosynthetic oxygen evolution. 1. Electron-paramagnetic resonance study of environment of manganese in Tris-washed chloroplasts. Biochimica et Biophysica Acta 357, 252–266.Google Scholar
Blankenship, RE, Tiede, DM, Barber, J, Brudvig, GW, Fleming, G, Ghirardi, M, Gunner, MR, Junge, W, Kramer, DM, Melis, A, Moore, TA, Moser, CC, Nocera, DG, Nozik, AJ, Ort, DR, Parson, WW, Prince, RC and Sayre, RT (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332, 805–809.Google Scholar
Boardman, NK and Anderson, JM (1964) Isolation from spinach chloroplasts of particles containing different proportions of chlorophyll alpha + chlorophyll beta + their possible role in light reactions of photosynthesis. Nature 203, 166.Google Scholar
Boska, M, Sauer, K, Buttner, W and Babcock, GT (1983) Similarity of EPR signal II f rise and P-680 + decay kinetics in Tris-washed chloroplast photosystem II preparations as a function of pH. Biochimica et Biophysica Acta 722, 327–330.Google Scholar
Bovi, D, Narzi, D and Guidoni, L (2013) The S-2 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 S-3 state. Angewandte Chemie-International Edition 52, 11744–11749.Google Scholar
Brena, B, Siegbahn, PEM and Agren, H (2012) Modeling near-edge fine structure X-ray spectra of the manganese catalytic site for water oxidation in photosystem II. Journal of the American Chemical Society 134, 17157–17167.Google Scholar
Brettel, K, Schlodder, E and Witt, HT (1984) Nanosecond reduction kinetics of photooxidized chlorophyll-aII (P 680) in single flashes as a probe for the electron pathway, H+-release and charge accumulation in the O 2 -evolving complex. Biochimica et Biophysica Acta 766, 403–415.Google Scholar
Brinkert, K, De Causmaecker, S, Krieger-Liszkay, A, Fantuzzi, A and Rutherford, AW (2016) Bicarbonate-induced redox tuning in photosystem II for regulation and protection. Proceedings of the National Academy of Sciences of the United States of America 113, 12144–12149.Google Scholar
Brudvig, GW and Crabtree, RH (1986) Mechanism for photosynthetic O-2 evolution. Proceedings of the National Academy of Sciences of the United States of America 83, 4586–4588.Google Scholar
Brudvig, GW and Crabtree, RH (1989) Bioinorganic chemistry of manganese related to photosynthetic oxygen evolution. Progress in Inorganic Chemistry 37, 99–142.Google Scholar
Burk, D, Schade, AL, Hunter, J and Warburg, O (1951) 3-Vessel and one-vessel manometric techniques for measuring Co2 And O-2 gas exchanges in respiration and photosynthesis. Symposia of the Society for Experimental Biology 5, 312–335.Google Scholar
Cardona, T, Murray, JW and Rutherford, AW (2015) Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Molecular Biology and Evolution 32, 1310–1328.Google Scholar
Cheniae, GM and Martin, IF (1967) Photoreactivation of manganese catalyst in photosynthetic oxygen evolution. Biochemical and Biophysical Research Communications 28, 89.Google Scholar
Cheniae, GM and Martin, IF (1970) Sites of function of manganese within photosystem-II – roles in O2 evolution and system-II. Biochimica et Biophysica Acta 197, 219.Google Scholar
Christou, G (1989) Manganese carboxylate chemistry and its biological relevance. Accounts of Chemical Research 22, 328–335.Google Scholar
Cinco, RM, Robblee, JH, Rompel, A, Fernandez, C, Yachandra, VK, Sauer, K and Klein, MP (1998) Strontium EXAFS reveals the proximity of calcium to the manganese cluster of oxygen-evolving photosystem II. Journal of Physical Chemistry B 102, 8248–8256.Google Scholar
Clausen, J and Junge, W (2004) Detection of an intermediate of photosynthetic water oxidation. Nature 430, 480–483.Google Scholar
Clausen, J, Winkler, S, Hays, AMA, Hundelt, M, Debus, RJ and Junge, W (2001) Photosynthetic water oxidation: mutations of D1-Glu189K, R and Q of Synechocystis sp. PCC6803 are without any influence on electron transfer rates at the donor side of photosystem II. Biochimica et Biophysica Acta 1506, 224–235.Google Scholar
Clausen, J, Debus, RJ and Junge, W (2004) Time-resolved oxygen production by PSII: chasing chemical intermediates. Biochimica et Biophysica Acta 1655, 184–194.Google Scholar
Clausen, J, Beckmann, K, Junge, W and Messinger, J (2005 a) Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution. Plant Physiology 139, 1444–1450.Google Scholar
Clausen, J, Junge, W, Dau, H and Haumann, M (2005 b) Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44, 12775–12779.Google Scholar
Cox, N and Messinger, J (2013) Reflections on substrate water and dioxygen formation. Biochimica et Biophysica Acta-Bioenergetics 1827, 1020–1030.Google Scholar
Cox, N, Retegan, M, Neese, F, Pantazis, DA, Boussac, A and Lubitz, W (2014) Electronic structure of the oxygenevolving complex in photosystem II prior to O–O bond formation. Science 345, 804–808.Google Scholar
Dau, H and Zaharieva, I (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation. Accounts of Chemical Research 42, 1861–1870.Google Scholar
Dau, H, Dittmer, J, Iuzzolino, L, Schiller, H, Dorner, W, Heinze, I, Sole, VA and Nolting, HF (1997) X-ray absorption linear dichroism spectroscopy (XALDS) on the photosystem II manganese complex: radiation damage and S-1-state K-edge spectra. Journal De Physique IV 7, 607–610.Google Scholar
Dau, H, Liebisch, P and Haumann, M (2003) X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers – potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Analytical and Bioanalytical Chemistry 376, 562–583.Google Scholar
Dau, H, Liebisch, P and Haumann, M (2004) The structure of the manganese complex of photosystem II in its dark-stable S-1-state-EXAFS results in relation to recent crystallographic data. Physical Chemistry Chemical Physics 6, 4781–4792.Google Scholar
Dau, H, Zaharieva, I and Haumann, M (2012) Recent developments in research on water oxidation by photosystem II. Current Opinion in Chemical Biology 16, 3–10.Google Scholar
De Paula, JC and Brudvig, GW (1985) Magnetic properties of manganese in the photosynthetic O2-evolving complex. Journal of the American Chemical Society 107, 2643–2648.Google Scholar
Debus, RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochimica et Biophysica Acta 1102, 269–352.Google Scholar
Debus, RJ, Barry, BA, Babcock, GT and Mcintosh, L (1988 a) Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proceedings of the National Academy of Sciences of the United States of America 85, 427–430.Google Scholar
Debus, RJ, Barry, BA, Sithole, I, Babcock, GT and Mcintosh, L (1988 b) Directed mutagenesis indicates that the donor to P-680+ in photosystem-II is tyrosine-161 of the D1 polypeptide. Biochemistry 27, 9071–9074.Google Scholar
Deisenhofer, J, Epp, O, Miki, K, Huber, R and Michel, H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 resolution. Nature 318, 618.Google Scholar
Dekker, JP, Plijter, JJ, Ouwehand, L and Van Gorkom, HJ (1984) Kinetics of manganese redox transitions in the oxygen evolving apparatus of photosynthesis. Biochimica et Biophysica Acta 767, 176–179.Google Scholar
Depaula, JC, Beck, WF and Brudvig, GW (1986) Magnetic-properties of manganese in the photosynthetic O-2-evolving complex. 2. Evidence for a manganese tetramer. Journal of the American Chemical Society 108, 4002–4009.Google Scholar
Dismukes, GC and Siderer, Y (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proceedings of the National Academy of Sciences of the United States of America 78, 274–278.Google Scholar
Döring, G, Stiehl, HH and Witt, HT (1967) A second chlorophyll reaction in the electron chain of photosynthesis – registration by repetitive excitation technique. Zeitschrift fur Naturforschung Part B-Chemie Biochemie Biophysik Biologie und Verwandten Gebiete, B 22, 639–644.Google Scholar
Duysens, LNM, Huiskamp, WJ, Vos, JJ and Vanderhart, JM (1956) Reversible changes in bacteriochlorophyll in purple bacteria upon illumination. Biochimica et Biophysica Acta 19, 188–190.Google Scholar
Duysens, LN, Kamp, BM and Amesz, J (1961) Two photochemical systems in photosynthesis. Nature 190, 510.Google Scholar
Emerson, R and Arnold, W (1932) The photochemical reaction in photosynthesis. The Journal of General Physiology 16, 191–205.Google Scholar
Engelmann, TW (1881) xxxx. Botanische Zeitung, 39.Google Scholar
Falkowski, P, Scholes, RJ, Boyle, E, Canadell, J, Canfield, D, Elser, J, Gruber, N, Hibbard, K, Hogberg, P, Linder, S, Mackenzie, FT, Moore, B III, Pedersen, T, Rosenthal, Y, Seitzinger, S, Smetacek, V and Steffen, W (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290, 291–296.Google Scholar
Ferreira, KN, Iverson, TM, Maghlaoui, K, Barber, J and Iwata, S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838.Google Scholar
Field, CB, Behrenfeld, MJ, Randerson, JT and Falkowski, P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240.Google Scholar
Förster, V and Junge, W (1985) Stoichiometry and kinetics of proton release upon photosynthetic water oxidation. Photochemistry and Photobiology 41, 183–190.Google Scholar
Förster, V, Hong, YQ and Junge, W (1981) Electron-transfer and proton pumping under excitation of dark-adapted chloroplasts with flashes of light. Biochimica et Biophysica Acta 638, 141–152.Google Scholar
Gao, Y, Akermark, T, Liu, JH, Sun, LC and Akermark, B (2009) Nucleophilic attack of hydroxide on a Mn-V oxo complex: a model of the O–O bond formation in the oxygen evolving complex of photosystem II. Journal of the American Chemical Society 131, 8726.Google Scholar
Gatt, P, Stranger, R and Pace, RJ (2011) Application of computational chemistry to understanding the structure and mechanism of the Mn catalytic site in photosystem II – a review. Journal of Photochemistry and Photobiology B-Biology 104, 80–93.Google Scholar
Gerken, S, Brettel, K, Schlodder, E and Witt, HT (1988) Optical characterization of the immediate electron donor to chlorophyll aII+ in oxygen-evolving photosystem II complexes. Tyrosine as possible electron carrier between chlorophyll aII and the water-oxidizing manganese complex. FEBS Letters 237, 69–75.Google Scholar
Ghanotakis, DF, Babcock, GT and Yocum, CF (1984 a) Calcium reconstitutes high-rates of oxygen evolution in polypeptide depleted photosystem-II preparations. FEBS Letters 167, 127–130.Google Scholar
Ghanotakis, DF, Babcock, GT and Yocum, CF (1984 b) Structural and catalytic properties of the oxygen-evolving complex. Correlation of polypeptide and manganese release with the behavior of Z+ in chloroplasts and a highly resolved preparation of the PS II complex. Biochimica et Biophysica Acta 765, 388–398.Google Scholar
Ghanotakis, DF, Babcock, GT and Yocum, CF (1985 a) On the role of water-soluble polypeptides (17, 23 kDa), calcium and chloride in photosynthetic oxygen evolution. FEBS Letters 192, 1–3.Google Scholar
Ghanotakis, DF, Babcock, GT and Yocum, CF (1985 b) Structure of the oxygen-evolving complex of photosystem-II – calcium and lanthanum compete for sites on the oxidizing side of photosystem-II which control the binding of water-soluble polypeptides and regulate the activity of the manganese complex. Biochimica et Biophysica Acta 809, 173–180.Google Scholar
Goodin, DB, Yachandra, VK, Britt, RD and Sauer, K (1984) The state of manganese in the photosynthetic apparatus 3. Light-induced changes in X-ray absorption (K-edge) energies of manganese in photosynthetic membranes. Biochimica et Biophysica Acta 767, 209–216.Google Scholar
Guo, Y, Li, H, He, LL, Zhao, DX, Gong, LD and Yang, ZZ (2017) The open-cubane oxo-oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S-4 state. Physical Chemistry Chemical Physics 19, 13909–13923.Google Scholar
Haumann, M and Junge, W (1994) Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. Biochemistry 33, 864–872.Google Scholar
Haumann, M, Bogershausen, O, Cherepanov, D, Ahlbrink, R and Junge, W (1997 a) Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during the redox reactions at the oxidizing side of photosystem II. Photosynthesis Research 51, 193–208.Google Scholar
Haumann, M, Mulkidjanian, AY and Junge, W (1997 b) The electrogenicities of electron and proton transfer at the oxidizing side of photosystem II. Biochemistry 36, 9304–9315.Google Scholar
Haumann, M, Muller, C, Liebisch, P, Iuzzolino, L, Dittmer, J, Grabolle, M, Neisius, T, Meyer-Klaucke, W and Dau, H (2005) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S-0→S-1, S-1→S-2, S-2→S-3, and S-3,S-4→S-0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44, 1894–1908.Google Scholar
Haumann, M, Grundmeier, A, Zaharieva, I and Dau, H (2008) Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements. Proceedings of the National Academy of Sciences of the United States of America 105, 17384–17389.Google Scholar
Hays, AM, Vassiliev, IR, Golbeck, JH and Debus, RJ (1998) Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37, 11352–11365.Google Scholar
Hellmich, J, Bommer, M, Burkhardt, A, Ibrahim, M, Kern, J, Meents, A, Muh, F, Dobbek, H and Zouni, A (2014) Native-like photosystem II superstructure at 2.44 angstrom resolution through detergent extraction from the protein crystal. Structure 22, 1607–1615.Google Scholar
Hill, R (1939) Oxygen produced by isolated chloroplasts. Proceedings of the Royal Society London 127, 192–210.Google Scholar
Hillier, W, Messinger, J and Wydrzynski, T (1998) Kinetic determination of the fast exchanging substrate water molecule in the S 3 state of photosystem II. Biochemistry 37, 16908–16914.Google Scholar
Hoganson, CW and Babcock, GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277, 1953–1956.Google Scholar
Hundelt, M, Hays, AM, Debus, RJ and Junge, W (1998) Oxygenic photosystem II: the mutation D1-D61N in Synechocystis sp. PCC 6803 retards S-state transitions without affecting electron transfer from Y Z to P 680+. Biochemistry, 37, 14450–14456.Google Scholar
Iuzzolino, L, Dittmer, J, D'RNER, W, Meyer-Klaucke, W and Dau, H (1998) X-ray absorption spectroscopy on layered photosystem II membrane particles suggests manganese-centered oxidation of the oxygen-evolving complex for the S 0-S 1, S 1-S 2 , and S 2-S 3 transitions of the water oxidizing complex. Biochemistry 37, 17112–17119.Google Scholar
Iwata, S and Barber, J (2004) Structure of photosystem II and molecular architecture of the oxygen-evolving centre. Current Opinion in Structural Biology 14, 447–453.Google Scholar
Jagendorf, AT and Uribe, E (1966) ATP formation caused by acid-base transition of spinach chloroplast. Proceedings of the National Academy of Sciences of the United States of America 55, 170–177.Google Scholar
Joliot, P and Joliot, A (1968) A polarographic method for detection of oxygen production and reduction of Hill reagent by isolated chloroplasts. Biochimica et Biophysica Acta 153, 625–634.Google Scholar
Joliot, P, Barbieri, G and Chabaud, R (1969) A new model of photochemical centers in system-2. Photochemistry and Photobiology 10, 309.Google Scholar
Jordan, P, Fromme, P, Witt, HT, Klukas, O, Saenger, W and Krauss, N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution. Nature 411, 909–917.Google Scholar
Junge, W (1970) Critical electric potential difference for photophosphorylation. Its relation to the chemiosmotic hypothesis and to the triggering requirements of the ATPase system. European Journal of Biochemistry 14, 582–592.Google Scholar
Junge, W (1977) Membrane potentials in photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 28, 503–536.Google Scholar
Junge, W and Nelson, N (2015) ATP synthase. Annual Review of Biochemistry 83, 631–657.Google Scholar
Junge, W and Rutherford, AW (2007) Obituary: Horst Tobias Witt (1922–2007). Nature 448, 425.Google Scholar
Junge, W and Witt, HT (1968) On the ion transport system of photosynthesis – investigation on a molecular level. Zeitschrift für Naturforschung 23, 244–254.Google Scholar
Junge, W, Rumberg, B and Schroeder, H (1970) Necessity of an electric potential difference and its use for photophosphorylation in short flash groups. European Journal of Biochemistry 14, 575–581.Google Scholar
Junge, W, Haumann, M, Ahlbrink, R, Mulkidjanian, A and Clausen, J (2002) Electrostatics and proton transfer in photosynthetic water oxidation. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 1407–1417.Google Scholar
Kamiya, N and Shen, JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-angstrom resolution. Proceedings of the National Academy of Sciences of the United States of America 100, 98–103.Google Scholar
Kern, J, Alonso-Mori, R, Hellmich, J, Tran, R, Hattne, J, Laksmono, H, Glockner, C, Echols, N, Sierra, RG, Sellberg, J, Lassalle-Kaiser, B, Gildea, RJ, Glatzel, P, Grosse-Kunstleve, RW, Latimer, MJ, Mcqueen, TA, Difiore, D, Fry, AR, Messerschmidt, M, Miahnahri, A, Schafer, DW, Seibert, MM, Sokaras, D, Weng, TC, Zwart, PH, White, WE, Adams, PD, Bogan, MJ, Boutet, S, Williams, GJ, Messinger, J, Sauter, NK, Zouni, A, Bergmann, U, Yano, J and Yachandra, VK (2012) Room temperature femtosecond X-ray diffraction of photosystem II microcrystals. Proceedings of the National Academy of Sciences of the United States of America 109, 9721–9726.Google Scholar
Kern, J, Alonso-Mori, R, Tran, R, Hattne, J, Gildea, RJ, Echols, N, Glockner, C, Hellmich, J, Laksmono, H, Sierra, RG, Lassalle-Kaiser, B, Koroidov, S, Lampe, A, Han, GY, Gul, S, Difiore, D, Milathianaki, D, Fry, AR, Miahnahri, A, Schafer, DW, Messerschmidt, M, Seibert, MM, Koglin, JE, Sokaras, D, Weng, TC, Sellberg, J, Latimer, MJ, Grosse-Kunstleve, RW, Zwart, PH, White, WE, Glatzel, P, Adams, PD, Bogan, MJ, Williams, GJ, Boutet, S, Messinger, J, Zouni, A, Sauter, NK, Yachandra, VK, Bergmann, U and Yano, J (2013) Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 340, 491–495.Google Scholar
Kern, J, Tran, R, Alonso-Mori, R, Koroidov, S, Echols, N, Hattne, J, Ibrahim, M, Gul, S, Laksmono, H, Sierra, RG, Gildea, RJ, Han, G, Hellmich, J, Lassalle-Kaiser, B, Chatterjee, R, Brewster, AS, Stan, CA, Gloeckner, C, Lampe, A, Difiore, D, Milathianaki, D, Fry, AR, Seibert, MM, Koglin, JE, Gallo, E, Uhlig, J, Sokaras, D, Weng, T-C, Zwart, PH, Skinner, DE, Bogan, MJ, Messerschmidt, M, Glatzel, P, Williams, GJ, Boutet, S, Adams, PD, Zouni, A, Messinger, J, Sauter, NK, Bergmann, U, Yano, J and Yachandra, VK (2014) Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. Nature Communications 5.Google Scholar
Kern, J, Chatterjee, R, Young, ID, Fuller, FD, Lassalle, L, Ibrahim, M, Gul, S, Fransson, T, Brewster, AS, Alonso-Mori, R, Hussein, R, Zhang, M, Douthit, L, De Lichtenberg, C, Cheah, MH, Shevela, D, Wersig, J, Seuffert, I, Sokaras, D, Pastor, E, Weninger, C, Kroll, T, Sierra, RG, Aller, P, Butryn, A, Orville, AM, Liang, MN, Batyuk, A, Koglin, JE, Carbajo, S, Boutet, S, Moriarty, NW, Holton, JM, Dobbek, H, Adams, PD, Bergmann, U, Sauter, NK, Zouni, A, Messinger, J, Yano, J and Yachandra, VK (2018) Structures of the intermediates of Kok's photosynthetic water oxidation clock. Nature 563, 421.Google Scholar
Kim, CJ and Debus, RJ (2017) Evidence from FTIR difference spectroscopy that a substrate H2O molecule for O-2 formation in photosystem II is provided by the Ca Ion of the catalytic Mn4CaO5 cluster. Biochemistry 56, 2558–2570.Google Scholar
Kirby, JA, Goodin, DB, Wydrzynski, T, Robertson, AS and Klein, MP (1981 a) State of manganese in the photosynthetic apparatus. 2. X-ray absorption-edge studies on manganese in photosynthetic membranes. Journal of the American Chemical Society 103, 5537–5542.Google Scholar
Kirby, JA, Robertson, AS, Smith, JP, Thompson, AC, Cooper, SR and Klein, MP (1981 b) State of manganese in the photosynthetic apparatus. 1. Extended X-ray absorption fine-structure studies on chloroplasts and di-μ-oxo-bridged dimanganese model compounds. Journal of the American Chemical Society 103, 5529–5537.Google Scholar
Klauss, A, Krivanek, R, Dau, H and Haumann, M (2009) Energetics and kinetics of photosynthetic water oxidation studied by photothermal beam deflection (PBD) experiments. Photosynthesis Research, 499–509.Google Scholar
Klauss, A, Haumann, M and Dau, H (2015) Seven steps of alternating electron and proton transfer in photosystem II water oxidation traced by time-resolved photothermal beam deflection at improved sensitivity. Journal of Physical Chemistry B 119, 2677–2689.Google Scholar
Kok, B (1956) Photosynthesis in flashing light. Biochimica et Biophysica Acta 21, 245–258.Google Scholar
Kok, B and Gott, W (1960) Activation spectra of 700-M-MU absorption change in photosynthesis. Plant Physiology 35, 802–808.Google Scholar
Kok, B, Forbush, B and Mcgloin, M (1970) Cooperation of charges in photosynthetic O2 evolution – I. A linear four-step mechanism. Photochemistry and Photobiology 11, 457–475.Google Scholar
Kolling, DR, Brown, TS, Ananyev, G and Dismukes, GC (2009) Photosynthetic oxygen evolution is not reversed at high oxygen pressures: mechanistic consequences for the water-oxidizing complex 2. Biochemistry 48, 1381–1389.Google Scholar
Koroidov, S, Shevela, D, Shutova, T, Samuelsson, G and Messinger, J (2014) Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation. Proceedings of the National Academy of Sciences of the United States of America 111, 6299–6304.Google Scholar
Krab, K, Kempe, H and Wikstrom, M (2011) Explaining the enigmatic K(M) for oxygen in cytochrome c oxidase: a kinetic model. Biochimica et Biophysica Acta 1807, 348–358.Google Scholar
Krewald, V, Retegan, M, Cox, N, Messinger, J, Lubitz, W, Debeer, S, Neese, F and Pantazis, DA (2015) Metal oxidation states in biological water splitting. Chemical Science 6, 1676–1695.Google Scholar
Krewald, V, Retegan, M, Neese, F, Lubitz, W, Pantazis, DA and Cox, N (2016) Spin state as a marker for the structural evolution of nature's water splitting catalyst. Inorganic Chemistry 55, 488–501.Google Scholar
Krishtalik, LI (1989) Energetics of photosynthetic oxygen evolution. Biofizika 34, 883–886.Google Scholar
Krishtalik, LI (1990) Activation energy of photosynthetic oxygen evolution: an attempt at theoretical analysis. Bioelectrochemistry and Bioenergetics 23, 249–263.Google Scholar
Krivanek, R, Dau, H and Haumann, M (2008) Enthalpy changes during photosynthetic water oxidation tracked by time-resolved calorimetry using a photothermal beam deflection technique. Biophysical Journal 94, 1890–1903.Google Scholar
Kulik, LV, Epel, B, Lubitz, W and Messinger, J (2005) Mn-55 pulse ENDOR at 34 GHz of the S-0 and S-2 states of the oxygen-evolving complex in photosystem II. Journal of the American Chemical Society 127, 2392–2393.Google Scholar
Kump, LR (2008) The rise of atmospheric oxygen. Nature 451, 277–278.Google Scholar
Kupitz, C, Basu, S, Grotjohann, I, Fromme, R, Zatsepin, NA, Rendek, KN, Hunter, MS, Shoeman, RL, White, TA, Wang, DJ, James, D, Yang, JH, Cobb, DE, Reeder, B, Sierra, RG, Liu, HG, Barty, A, Aquila, AL, Deponte, D, Kirian, RA, Bari, S, Bergkamp, JJ, Beyerlein, KR, Bogan, MJ, Caleman, C, Chao, TC, Conrad, CE, Davis, KM, Fleckenstein, H, Galli, L, Hau-Riege, SP, Kassemeyer, S, Laksmono, H, Liang, MN, Lomb, L, Marchesini, S, Martin, AV, Messerschmidt, M, Milathianaki, D, Nass, K, Ros, A, Roy-Chowdhury, S, Schmidt, K, Seibert, M, Steinbrener, J, Stellato, F, Yan, LF, Yoon, C, Moore, TA, Moore, AL, Pushkar, Y, Williams, GJ, Boutet, S, Doak, RB, Weierstall, U, Frank, M, Chapman, HN, Spence, JCH and Fromme, P (2014) Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513, 261.Google Scholar
Kusunoki, M (2007) Mono-manganese mechanism of the photosystem II water splitting reaction by a unique Mn4Ca cluster. Biochimica et Biophysica Acta-Bioenergetics 1767, 484–492.Google Scholar
Kusunoki, M (2011) S-1-state Mn4Ca complex of photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence. Journal of Photochemistry and Photobiology B-Biology 104, 100–110.Google Scholar
Latimer, MJ, Derose, VJ, Mukerji, I, Yachandra, VK, Sauer, K and Klein, MP (1995) Evidence for the proximity of calcium to the manganese cluster of photosystem II: determination by X-ray absorption spectroscopy. Biochemistry 34, 10898–10909.Google Scholar
Lavergne, J and Junge, W (1993) Proton release during the redox cycle of the water oxidase. Photosynthesis Research 38, 279–296.Google Scholar
Li, XC, Sproviero, EM, Ryde, U, Batista, VS and Chen, GJ (2013) Theoretical EXAFS studies of a model of the oxygen-evolving complex of photosystem II obtained with the quantum cluster approach. International Journal of Quantum Chemistry 113, 474–478.Google Scholar
Loll, B, Kern, J, Saenger, W, Zouni, A and Biesiadka, J (2005) Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of photosystem II. Nature 438, 1040–1044.Google Scholar
Mcevoy, JP, Gascon, JA, Batista, VS and Brudvig, GW (2005) The mechanism of photosynthetic water splitting. Photochemical & Photobiological Sciences 4, 940–949.Google Scholar
Menke, W (1962) Structure and chemistry of plastids. Annual Review of Plant Physiology 13, 27–44.Google Scholar
Messinger, J (2000) Towards understanding the chemistry of photosynthetic oxygen evolution: dynamic structural changes, redox states and substrate water binding of the Mn cluster in photosystem II. Biochimica et Biophysica Acta-Bioenergetics 1459, 481–488.Google Scholar
Messinger, J (2004) Evaluation of different mechanistic proposals for water oxidation in photosynthesis on the basis of Mn4OxCa structures for the catalytic site and spectroscopic data. Physical Chemistry Chemical Physics 6, 4764–4771.Google Scholar
Messinger, J, Badger, M and Wydrzynski, T (1995) Detection of one slowly exchanging substrate water molecule in the S 3 state of photosystem II. Proceedings of the National Academy of Sciences of the United States of America 92, 3209–3213.Google Scholar
Messinger, J, Robblee, JH, Bergmann, U, Fernandez, C, Glatzel, P, Visser, H, Cinco, RM, Mcfarlane, KL, Bellacchio, E, Pizarro, SA, Cramer, SP, Sauer, K, Klein, MP and Yachandra, VK (2001) Absence of Mn-centered oxidation in the S-2→S-3 transition: implications for the mechanism of photosynthetic water oxidation. Journal of the American Chemical Society 123, 7804–7820.Google Scholar
Meyer, B, Schlodder, E, Dekker, JP and Witt, HT (1989) O2 evolution and Chl a II + (P-680+) nanosecond reduction kinetics in single flashes as a function of pH. Biochimica et Biophysica Acta 974, 36–43.Google Scholar
Mitchell, P (1961) Coupling of photophosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191, 144–148.Google Scholar
Mitchell, P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Physiological Reviews 41, 445–502.Google Scholar
Narzi, D, Bovi, D and Guidoni, L (2014) Pathway for Mn-cluster oxidation by tyrosine-Z in the S-2 state of photosystem II. Proceedings of the National Academy of Sciences of the United States of America 111, 8723–8728.Google Scholar
Nilsson, H, Krupnik, T, Kargul, J and Messinger, J (2014 a) Substrate water exchange in photosystem II core complexes of the extremophilic red alga Cyanidioschyzon merolae. Biochimica et Biophysica Acta-Bioenergetics 1837, 1257–1262.Google Scholar
Nilsson, H, Rappaport, F, Boussac, A and Messinger, J (2014 b) Substrate-water exchange in photosystem II is arrested before dioxygen formation. Nature Communications 5:4305, 1–7.Google Scholar
Nilsson, H, Cournac, L, Rappaport, F, Messinger, J and Lavergne, J (2016) Estimation of the driving force for dioxygen formation in photosynthesis. Biochimica et Biophysica Acta-Bioenergetics 1857, 23–33.Google Scholar
Nitschke, W and Rutherford, AW (1991) Photosynthetic reaction centers: variations on a common structural theme? Trends in Biochemical Sciences 16, 241–245.Google Scholar
Orsi, F, Muratori, M, Rocco, M, Colombo, E and Rizzoni, G (2016) A multi-dimensional well-to-wheels analysis of passenger vehicles in different regions: primary energy consumption, CO2 emissions, and economic cost. Applied Energy 169, 197–209.Google Scholar
Ort, DR, Merchant, SS, Alric, J, Barkan, A, Blankenship, RE, Bock, R, Croce, R, Hanson, MR, Hibberd, JM, Long, SP, Moore, TA, Moroney, J, Niyogi, KK, Parry, MAJ, Peralta-Yahya, PP, Prince, RC, Redding, KE, Spalding, MH, Van Wijk, KJ, Vermaas, WFJ, Von Caemmerer, S, Weber, APM, Yeates, TO, Yuan, JS and Zhu, XG (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proceedings of the National Academy of Sciences of the United States of America 112, 8529–8536.Google Scholar
Pecoraro, VL, Baldwin, MJ, Caudle, MT, Hsieh, WY and Law, NA (1998) A proposal for water oxidation in photosystem II. Pure and Applied Chemistry 70, 925–929.Google Scholar
Peloquin, JM and Britt, RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochimica et Biophysica Acta 1503, 96–111.Google Scholar
Petrie, S, Gatt, P, Stranger, R and Pace, RJ (2012) Modelling the metal atom positions of the photosystem II water oxidising complex: a density functional theory appraisal of the 1.9 angstrom resolution crystal structure. Physical Chemistry Chemical Physics 14, 11333–11343.Google Scholar
Planavsky, NJ, Asael, D, Hofmann, A, Reinhard, CT, Lalonde, SV, Knudsen, A, Wang, XL, Ossa, FO, Pecoits, E, Smith, AJB, Beukes, NJ, Bekker, A, Johnson, TM, Konhauser, KO, Lyons, TW and Rouxel, OJ (2014) Evidence for oxygenic photosynthesis half a billion years before the great oxidation event. Nature Geoscience 7, 283–286.Google Scholar
Priestley, J (1772) Observations of different kinds of air. Philosophical Transactions of the Royal Society of London 62, 147–264.Google Scholar
Rapatskiy, L, Cox, N, Savitsky, A, Ames, WM, Sander, J, Nowaczyk, MM, Rogner, M, Boussac, A, Neese, F, Messinger, J and 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 the American Chemical Society 134, 16619–16634.Google Scholar
Raven, JA and Larkum, AWD (2007) Are there ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations? Photosynthesis Research 94, 31–42.Google Scholar
Renger, G (1977) A model for the molecular mechanism of photosynthetic oxygen evolution. FEBS Letters 81, 223–228.Google Scholar
Renger, G (1987) Mechanistic aspects of photosynthetic water cleavage. Photosynthetica 21, 203–224.Google Scholar
Retegan, M, Cox, N, Lubitz, W, Neese, F and Pantazis, DA (2014) The first tyrosyl radical intermediate formed in the S-2-S-3 transition of photosystem II. Physical Chemistry Chemical Physics 16, 11901–11910.Google Scholar
Retegan, M, Krewald, V, Mamedov, F, Neese, F, Lubitz, W, Cox, N and Pantazis, DA (2016) A five-coordinate Mn(IV) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding. Chemical Science 7, 72–84.Google Scholar
Rhee, KH, Morriss, EP, Barber, J and Kuhlbrandt, W (1998) Three-dimensional structure of the plant photosystem II reaction centre at 8 angstrom resolution. Nature 396, 283–286.Google Scholar
Rieger, B, Junge, W and Busch, KB (2014) Lateral pH gradient between OXPHOS complex IV and F(0)F(1) ATP-synthase in folded mitochondrial membranes. Nature Communications 5, 3103.Google Scholar
Robblee, JH, Messinger, J, Cinco, RM, Mcfarlane, KL, Fernandez, C, Pizarro, SA, Sauer, K and Yachandra, VK (2002) The Mn cluster in the S-0 state of the oxygen-evolving complex of photosystem II studied by EXAFS spectroscopy: are there three di-mu-oxo-bridged Mn-2 moieties in the tetranuclear Mn complex? Journal of the American Chemical Society 124, 7459–7471.Google Scholar
Roelofs, TA, Liang, W, Latimer, MJ, Cinco, RM, Rompel, A, Andrews, JC, Sauer, K, Yachandra, VK and Klein, M (1996) Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex. Proceedings of the National Academy of Sciences of the United States of America 93, 3335–3340.Google Scholar
Rögner, M, Dekker, JP, Boekema, EJ and Witt, HT (1987) Size, shape and mass of the oxygen-evolving photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Letters 219, 207–211.Google Scholar
Ruben, SR, Kamen, M and Hyde, JL (1941) Heavy oxygen (O18) as a tracer in the study of photosynthesis. Journal of the American Chemical Society 63, 877–879.Google Scholar
Rutherford, AW, Osyczka, A and Rappaport, F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O(2). FEBS Letters 586, 603–616.Google Scholar
Saito, T, Yamanaka, S, Kanda, K, Isobe, H, Takano, Y, Shigeta, Y, Umena, Y, Kawakami, K, Shen, JR, Kamiya, N, Okumura, M, Shoji, M, Yoshioka, Y and Yamaguchi, K (2012) Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn4O5 cluster of PSII refined to 1.9 angstrom X-ray resolution. International Journal of Quantum Chemistry 112, 253–276.Google Scholar
Sakamoto, H, Shimizu, T, Nagao, R and Noguchi, T (2017) Monitoring the reaction process during the S-2→ S-3 transition in photosynthetic water oxidation using time-resolved infrared spectroscopy. Journal of the American Chemical Society 139, 2022–2029.Google Scholar
Sauer, K (1980) A role for manganese in oxygen evolution in photosynthesis. Accounts of Chemical Research 13, 249–256.Google Scholar
Schatz, GH, Brock, H and Holzwarth, AR (1987) Picosecond kinetics of fluorescence and absorbency changes in photosystem-ii particles excited at low photon density. Proceedings of the National Academy of Sciences of the United States of America 84, 8414–8418.Google Scholar
Schatz, GH, Brock, H and Holzwarth, AR (1988) Kinetic and energetic model for the primary processes in photosystem-ii. Biophysical Journal 54, 397–405.Google Scholar
Schiller, H, Dittmer, J, Iuzzolino, L, Dorner, W, Meyer-Klaucke, W, Sole, VA, Nolting, HF and Dau, H (1998) Structure and orientation of the oxygen-evolving manganese complex of green algae and higher plants investigated by X-ray absorption linear dichroism spectroscopy on oriented photosystem II membrane particles. Biochemistry 37, 7340–7350.Google Scholar
Schliephake, W, Junge, W and Witt, HT (1968) Correlation between field formation, proton translocation, and the light reactions in photosynthesis. Zeitschrift für Naturforschung 23, 1571–1578.Google Scholar
Schlodder, E, Brettel, K, Schatz, GH and Witt, HT (1984) Analysis of the Chl- a II+ reduction kinetics with nanosecond time resolution in oxygen-evolving photosystem II particles from Synechococcus at 680 and 824 nm. Biochimica et Biophysica Acta 765, 178–185.Google Scholar
Schönknecht, G, Althoff, G and Junge, W (1990) The electric unit size of thylakoid membranes. FEBS Letters 277, 65–68.Google Scholar
Schuth, N, Zaharieva, I, Chernev, P, Berggren, G, Anderlund, M, Styring, S, Dau, H and Haumann, M (2018) K alpha X-ray emission spectroscopy on the photosynthetic oxygen-evolving complex supports manganese oxidation and water binding in the S-3 state. Inorganic Chemistry 57, 10424–10430.Google Scholar
Shen, JR and Kamiya, N (2000) Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochemistry 39, 14739–14744.Google Scholar
Shevela, D, Beckmann, K, Clausen, J, Junge, W and Messinger, J (2011) Membrane-inlet mass spectrometry reveals a high driving force for oxygen production by photosystem II. Proceedings of the National Academy of Sciences of the United States of America 108, 3602–3607.Google Scholar
Shevela, D, Eaton-Rye, JJ, Shen, JR and Govindjee, G (2012) Photosystem II and the unique role of bicarbonate: a historical perspective. Biochimica et Biophysica Acta 1817, 1134–1151.Google Scholar
Siegbahn, PE (2008 a) Mechanism and energy diagram for O–O bond formation in the oxygen-evolving complex in photosystem II. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 1221–1228.Google Scholar
Siegbahn, PE (2008 b) A structure-consistent mechanism for dioxygen formation in photosystem II. Chemistry 14, 8290–8302.Google Scholar
Siegbahn, PE (2009) Structures and energetics for O2 formation in photosystem II. Accounts of Chemical Research 42, 1871–1880.Google Scholar
Siegbahn, PEM (2000) Theoretical models for the oxygen radical mechanism of water oxidation and of the water oxidizing complex of photosystem II. Inorganic Chemistry 39, 2923–2935.Google Scholar
Siegbahn, PEM (2006) O–O bond formation in the S-4 state of the oxygen-evolving complex in photosystem II. Chemistry-A European Journal 12, 9217–9227.Google Scholar
Siegbahn, PEM (2013 a) Substrate water exchange for the oxygen evolving complex in PSII in the S-1, S-2, and S-3 states. Journal of the American Chemical Society 135, 9442–9449.Google Scholar
Siegbahn, PEM (2013 b) Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O–O bond formation and O-2 release. Biochimica et Biophysica Acta-Bioenergetics 1827, 1003–1019.Google Scholar
Siegbahn, PEM (2017) Nucleophilic water attack is not a possible mechanism for O–O bond formation in photosystem II. Proceedings of the National Academy of Sciences of the United States of America 114, 4966–4968.Google Scholar
Siegbahn, PEM and Blomberg, MRA (2014) Energy diagrams for water oxidation in photosystem II using different density functionals. Journal of Chemical Theory and Computation 10, 268–272.Google Scholar
Siegbahn, PEM and Crabtree, RH (1999) Manganese oxyl radical intermediates and O–O bond formation in photosynthetic oxygen evolution and a proposed role for the calcium cofactor in photosystem II. Journal of the American Chemical Society 121, 117–127.Google Scholar
Sjoholm, J, Bergstrand, J, Nilsson, T, Sachl, R, Von Ballmoos, C, Widengren, J and Brzezinski, P (2017) The lateral distance between a proton pump and ATP synthase determines the ATP-synthesis rate. Scientific Reports 7:2926, 1–12.Google Scholar
South, PF, Cavanagh, AP, Liu, HW and Ort, DR (2018) Improving crop productivity by bypassing photorespiration: a synthetic biology approach. In Vitro Cellular & Developmental Biology-Animal 54, S18–S19.Google Scholar
Spector, MB and Winget, GD (1979) Chloroplast membrane-protein required for the photosynthetic oxidation of water. Ohio Journal of Science 79, 21–21.Google Scholar
Sproviero, EM, Gascon, JA, Mcevoy, JP, Brudvig, GW and Batista, VS (2006) QM/MM models of the O-2-evolving complex of photosystem II. Journal of Chemical Theory and Computation 2, 1119–1134.Google Scholar
Sproviero, EM, Gascon, JA, Mcevoy, JP, Brudvig, GW and Batista, VS (2008) Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. Journal of the 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 and Shen, J-R (2015) Native structure of photosystem II at 1.95 angstrom resolution viewed by femtosecond X-ray pulses. Nature 517, 99–U265.Google Scholar
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, LJ, Sakamoto, T, Motomura, T, Chen, JH, 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 and Shen, JR (2017) Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543, 131.Google Scholar
Suzuki, H, Sugiura, M and Noguchi, T (2008) Monitoring water reactions during the S-state cycle of the photosynthetic water-oxidizing center: detection of the DOD bending vibrations by means of Fourier transform infrared spectroscopy. Biochemistry 47, 11024–11030.Google Scholar
Tanaka, A, Fukushima, Y and Kamiya, N (2017) Two different structures of the oxygen-evolving complex in the same polypeptide frameworks of photosystem II. Journal of the American Chemical Society 139, 1718–1721.Google Scholar
Tommos, C and Babcock, GT (1998) Oxygen production in nature: a light-driven metalloradical enzyme process. Accounts of Chemical Research 31, 18–25.Google Scholar
Torchio, MF and Santarelli, MG (2010) Energy, environmental and economic comparison of different powertrain/fuel options using well-to-wheels assessment, energy and external costs European market analysis. Energy 35, 4156–4171.Google Scholar
Tran, R, Kern, J, Hattne, J, Koroidov, S, Hellmich, J, Alonso-Mori, R, Sauter, NK, Bergmann, U, Messinger, J, Zouni, A, Yano, J and Yachandra, VK (2014) The Mn4Ca photosynthetic water-oxidation catalyst studied by simultaneous X-ray spectroscopy and crystallography using an X-ray free-electron laser. Philosophical Transactions of the Royal Society B-Biological Sciences 369:20130324, 1–5.Google Scholar
Umena, Y, Kawakami, K, Shen, J-R and Kamiya, N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature 473, 55–U65.Google Scholar
Wang, M, Han, J, Dunn, JB, Cai, H and Elgowainy, A (2012) Well-to-wheels energy use and greenhouse gas emissions of ethanol from corn, sugarcane and cellulosic biomass for US use. Environmental Research Letters 7:045905, 1–13.Google Scholar
Warburg, ONE (1922). Über den Energieumsatz bei der Kohlensäureassimilation. Zeitschrift für Physikalische Chemie 102, 235–266.Google Scholar
Warburg, O, Krippahl, G and Jetschma, C (1965) Widerlegung der Photolyse des Wassers und Beweis der Photolyse der Kohlensäure nach Versuchen mit lebender Chlorella und den Hill-Reagentien Nitrat und K3Fe(Cn)6. Zeitschrift für Naturforschung B 20, 993–996.Google Scholar
Wieghardt, K (1989) The active-sites in manganese-containing metalloproteins and inorganic model complexes. Angewandte Chemie-International Edition in English 28, 1153–1172.Google Scholar
Witt, HT and Moraw, R (1959) Untersuchungen über die Primärvorgänge bei der Photosynthese. I. Mitteilung. Zeitschrift für Physikalische Chemie 20, 253–282.Google Scholar
Witt, HT, Mueller, A and Rumberg, B (1961 a) Experimental evidence for the mechanism of photosynthesis. Nature 191, 194–195.Google Scholar
Witt, HT, Mueller, A and Rumberg, B (1961 b) Oxidized cytochrome and chlorophyll C2-plus in photosynthesis. Nature 192, 967–969.Google Scholar
Witt, I, Witt, HT, Difiore, D, Rogner, M, Hinrichs, W, Saenger, W, Granzin, J, Betzel, C and Dauter, Z (1988) X-ray characterization of single-crystals of the reaction center-I of water splitting photosynthesis. Berichte Der Bunsen-Gesellschaft-Physical Chemistry Chemical Physics 92, 1503–1506.Google Scholar
Wydrzynski, T and Sauer, K (1980) Periodic changes in the oxidation-state of manganese in photosynthetic oxygen evolution upon illumination with flashes. Biochimica et Biophysica Acta 589, 56–70.Google Scholar
Yachandra, VK, Guiles, RD, Mcdermott, AE, Cole, JL, Britt, RD, Dexheimer, SL, Sauer, K and Klein, MP (1987 a) Comparison of the structure of the manganese complex in the S1 and S2 states of the photosynthetic O-2-evolving complex: an X-ray absorption spectroscopy study. Biochemistry 26, 5974–5981.Google Scholar
Yachandra, VK, Guiles, RD, Mcdermott, AE, Cole, JL, Britt, RD, Dexheimer, SL, Sauer, K and Klein, MP (1987 b) The state of manganese in the photosynthetic apparatus. 7. Comparison of the structure of the manganese complex in the s-1 and s-2 states of the photosynthetic o-2-evolving complex – an X-ray absorption-spectroscopy study. Biochemistry 26, 5974–5981.Google Scholar
Yachandra, VK, Derose, VJ, Latimer, MJ, Mukerji, I, Sauer, K and Klein, MP (1993) Where plants make oxygen: a structural model for the photosynthetic oxygen-evolving manganese cluster. Science 260, 675–679.Google Scholar
Yachandra, VK, Sauer, K and Klein, MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chemical Reviews 96, 2927–2950.Google Scholar
Yamanaka, S, Isobe, H, Kanda, K, Saito, T, Umena, Y, Kawakami, K, Shen, JR, Kamiya, N, Okumura, M, Nakamura, H and 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 angstrom X-ray resolution. Chemical Physics Letters 511, 138–145.Google Scholar
Yano, J, Kern, J, Irrgang, KD, Latimer, MJ, Bergmann, U, Glatzel, P, Pushkar, Y, Biesiadka, J, Loll, B, Sauer, K, Messinger, J, Zouni, A and Yachandra, VK (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, MJ, Pushkar, Y, Biesiadka, J, Loll, B, Saenger, W, Messinger, J, Zouni, A and Yachandra, VK (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314, 821–825.Google Scholar
Yocum, CF (1991) Calcium activation of photosynthetic water oxidation. Biochimica et Biophysica Acta 1059, 1–15.Google Scholar
Young, ID, Ibrahim, M, Chatterjee, R, Gul, S, Fuller, FD, Koroidov, S, Brewster, AS, Tran, R, Alonso-Mori, R, Kroll, T, Michels-Clark, T, Laksmono, H, Sierra, RG, Stan, CA, Hussein, R, Zhang, M, Douthit, L, Kubin, M, De Lichtenberg, C, Pham, LV, Nilsson, H, Cheah, MH, Shevela, D, Saracini, C, Bean, MA, Seuffert, I, Sokaras, D, Weng, TC, Pastor, E, Weninger, C, Fransson, T, Lassalle, L, Brauer, P, Aller, P, Docker, PT, Andi, B, Orville, AM, Glownia, JM, Nelson, S, Sikorski, M, Zhu, DL, Hunter, MS, Lane, TJ, Aquila, A, Koglin, JE, Robinson, J, Liang, MN, Boutet, S, Lyubimov, AY, Uervirojnangkoorn, M, Moriarty, NW, Liebschner, D, Afonine, PV, Waterman, DG, Evans, G, Wernet, P, Dobbek, H, Weis, WI, Brunger, AT, Zwart, PH, Adams, PD, Zouni, A, Messinger, J, Bergmann, U, Sauter, NK, Kern, J, Yachandra, VK and Yano, J (2016) Structure of photosystem II and substrate binding at room temperature. Nature 540, 453.Google Scholar
Zaharieva, I, Chernev, P, Berggren, G, Anderlund, M, Styring, S, Dau, H and Haumann, M (2016 a) Room-temperature energy-sampling K beta X-ray emission spectroscopy of the Mn4Ca complex of photosynthesis reveals three manganese-centered oxidation steps and suggests a coordination change prior to O-2 formation. Biochemistry 55, 4197–4211.Google Scholar
Zaharieva, I, Dau, H and Haumann, M (2016 b) Sequential and coupled proton and electron transfer events in the S-2→S-3 transition of photosynthetic water oxidation revealed by time-resolved X-ray absorption spectroscopy. Biochemistry 55, 6996–7004.Google Scholar
Zhang, CX, Chen, CH, Dong, HX, Shen, JR, Dau, H and Zhao, JQ (2015) A synthetic Mn4Ca-cluster mimicking the oxygen-evolving center of photosynthesis. Science 348, 690–693.Google Scholar
Zhang, M, Bommer, M, Chatterjee, R, Hussein, R, Yano, J, Dau, H, Kern, J, Dobbek, H and Zouni, A (2017) Structural insights into the light-driven auto-assembly process of the water oxidizing Mn4CaO5-cluster in photosystem II. Elife 6:e26933, 1–20.Google Scholar
Zheng, M and Dismukes, GC (1996) Orbital configuration of the valence electrons, ligand field symmetry, and manganese oxidation states of the photosynthetic water oxidizing complex: analysis of the S2 state multiline EPR signals. Inorganic Chemistry 35, 3307–3319.Google Scholar
Zhu, XG, Long, SP and Ort, DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Current Opinion in Biotechnology 19, 153–159.Google Scholar
Zouni, A, Jordan, R, Schlodder, E, Fromme, P and Witt, HT (2000) First photosystem II crystals capable of water oxidation. Biochimica et Biophysica Acta 1457, 103–105.Google Scholar
Zouni, A, Witt, HT, Kern, J, Fromme, P, Krauss, N, Saenger, W and Orth, P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 resolution. Nature 409, 739–743.Google Scholar