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Mechanism of Photosynthetic Oxygen Production

  • Chapter
Photosystem II

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 22))

Summary

This chapter deals with the mechanism of photosynthetic water oxidation that leads to O2 formation in Photosystem II (PS II). After a brief introduction to the structure and function of the PS II complex, the S-state cycle (Kok model) is outlined and the structure and oxidation states of the catalytic Mn4OxCa complex are summarized. We then cover in detail the current information concerning substrate water binding and consider energetic and kinetic aspects of photosynthetic water oxidation. On that basis, we discuss several recent mechanistic proposals for O-O bond formation in PS II and summarize our current perceptions in a novel mechanistic proposal for photosynthetic water oxidation.

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References

  • Ahlbrink R, Haumann M, Cherepanov D, Bögershausen O, Mulkidjanian A and Junge W (1998) Function of tyrosine Z in water oxidation by Photosystem II: Electrostatical promoter instead of hydrogen abstractor. Biochemistry 37: 1131–1142

    Article  CAS  PubMed  Google Scholar 

  • Åhrling KA, Peterson S and Styring S (1997) An oscillating manganese electron paramagnetic resonance signal from the S0 state of the oxygen evolving complex in Photosystem II. Biochemistry 36: 13148–13152

    CAS  PubMed  Google Scholar 

  • Åhrling KA, Evans MCW, Nugent JHA and Pace RJ (2004) The two forms of the S2 state multiline signal in Photosystem II: effect of methanol and ethanol. Biochim Biophys Acta 1656: 66–77

    PubMed  Google Scholar 

  • Ananyev GM, Zaltsman L, Vasko C and Dismukes GC (2001) The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim Biophys Acta 1503: 52–68

    CAS  PubMed  Google Scholar 

  • Anderson JM (2001) Does functional Photosystem II complex have an oxygen channel? FEBS Lett 488: 1–4

    Article  CAS  PubMed  Google Scholar 

  • Aznar CP and Britt RD (2002) Simulations of the 1H electron spin echo-electron nuclear double resonance and 2H electron spin echo envelope modulation spectra of exchangeable hydrogen nuclei coupled to the S2 state Photosystem II manganese cluster. Philos Trans Roy Soc London B 357: 1359–1365

    CAS  Google Scholar 

  • Babcock GT, Blankenship RE and Sauer K (1976) Reaction kinetics for positive charge accumulation on the water side of chloroplast Photosystem II. FEBS Lett 61: 286–289

    CAS  PubMed  Google Scholar 

  • Bader KP, Renger G and Schmid GH (1993) A mass-spectrometric analysis of the water splitting reaction. Photosynth Res 38:355–361

    Article  CAS  Google Scholar 

  • Baranov SV, Ananyev GM, Klimov VV and Dismukes GC (2000) Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese depleted Photosystem II: A proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis. Biochemistry 39: 6060–6065

    Article  CAS  PubMed  Google Scholar 

  • Beck WF and Brudvig GW (1986) Binding of amines to the O2 evolving center of Photosystem II. Biochemistry 25: 6479–6486

    Article  CAS  PubMed  Google Scholar 

  • Beck WF and Brudvig GW (1988a) Resolution of the paradox of ammonia and hydroxylamine as substrate analogs for the water-oxidation reaction catalyzed by Photosystem II. J Am Chem Soc 110: 1517–1523

    CAS  Google Scholar 

  • Beck WF and Brudvig GW (1988b) Ligand substitution reactions of the oxygen evolving center of Photosystem II. Chem Script 28A: 93–98

    Google Scholar 

  • Beck WF, Depaula JC and Brudvig GW(1986) Ammonia binds to the manganese site of the O2 Revolving complex of Photosystem II in the S2 state. J Am Chem Soc 108: 4018–4022

    Article  CAS  Google Scholar 

  • Bergmann U, Grush MM, Home CR, DeMarois P, Penner-Hahn JE, Yocum CF, Wright DW, Dubé CE, Armstrong WH, Christou G, Eppley HJ and Cramer SP (1998) Characterization of the Mn oxidation states in Photosystem II by Kß X-ray fluorescence spectroscopy. J Phys Chem B 102: 8350–8352

    Article  CAS  Google Scholar 

  • Bernarding J, Eckert HJ, Eichler HJ, Napiwotzki A and Renger G (1994) Kinetic studies on the stabilization of the primary radical pair P680+ Pheo- in different Photosystem II preparations from higher plants. Photochem Photobiol 59: 566–573

    CAS  Google Scholar 

  • Biesiadka J, Loll B, Kern J, Irrgang K-D and Zouni A (2004) Crystal structure of cyanobacterial Photosystem II at 3.2 Å resolution: A closer look at the Mn-cluster. Phys Chem Chem Phys 6: 4733–4736

    Article  CAS  Google Scholar 

  • Blomberg MRA, Siegbahn PEM, Styring S, Babcock GT, Åkermark B and Korall P (1997) A quantum chemical study of hydrogen abstraction from manganese coordinated water by a tyrosyl radical: A model for water oxidation in Photosystem II. J Am Chem Soc 119: 8285–8292

    Article  CAS  Google Scholar 

  • Bögershausen O, Haumann M and Junge W (1996) Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during transitions S2 to S3 and S3 to S4 to S0. Ber Bunsen Phys Chem 100: 1987–1992

    Google Scholar 

  • Bouges B (1971) Action de faibles concentrations d’hydroxylamine sur remission d’oxygene des algues chlorella et des chloroplastes d’epinards. Biochim Biophys Acta 936: 228–235

    Google Scholar 

  • Boussac A and Etienne AL (1982) Oxido-reduction kinetics of Signal IIslow in Tris washed chloroplasts. Biochem Biophys Res Commun 109: 1200–1205

    CAS  PubMed  Google Scholar 

  • Boussac A and Rutherford AW (1988) Ca2+ binding to the oxygen evolving enzyme varies with the redox state of the Mn cluster. FEBS Lett 236: 432–436

    Article  CAS  Google Scholar 

  • Boussac A, Rutherford AW and Styring S (1990) Interaction of ammonia with the water splitting enzyme of Photosystem II. Biochemistry 29: 24–32

    Article  CAS  PubMed  Google Scholar 

  • Brettel K, Schlodder E and Witt HT (1984) Nanosecond reduction kinetics of photooxidised chlorophyll aII (P680) in single flashes as a probe for the electron pathway, H+ release and charge accumulation in the O2 evolving complex. Biochim Biophys Acta 766: 403–415

    CAS  Google Scholar 

  • Britt RD (1996) Oxygen evolution. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 137–164. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Britt RD, Zimmermann J-L, Sauer K and Klein MP (1989) Ammonia binds to the catalytic Mn of the oxygen evolving complex of Photosystem II: Evidence by electron spin-echo envelope modulation spectroscopy. J Am Chem Soc 111: 3522–3532

    Article  CAS  Google Scholar 

  • Britt RD, Peloquin JM and Campbell KA (2000) Pulsed and parallel-polarization EPR characterization of the Photosystem II oxygen evolving complex. An Rev Biophys Biomol Struct 29: 463–495

    CAS  Google Scholar 

  • Britt RD, Campbell KA, Peloquin JM, Gilchrist ML, Aznar CP, Dicus MM, Robblee J and Messinger J (2004) Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: Implications as to water oxidation mechanisms. Biochim Biophys Acta 1655: 158–171

    CAS  PubMed  Google Scholar 

  • Burnap RL, Shen J-R, Jursinic PA, Inoue Y and Sherman LA (1992) Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese stabilizing protein of Photosystem II. Biochemistry 31: 7404–7410

    Article  CAS  PubMed  Google Scholar 

  • Buser CA, Diner BA and Brudvig GW (1992) Photooxidation of cytochrome b559 in oxygen evolving Photosystem II. Biochemistry 31: 11449–11459

    CAS  PubMed  Google Scholar 

  • Carell TG, Tyryshkin AM and Dismukes GC (2002) An evaluation of structural models for the photosynthetic water oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem 7: 2–22

    Google Scholar 

  • Caudle MT and Pecoraro VL (1997) Thermodynamic viability of hydrogen atom transfer from water coordinated to the oxygen evolving complex of Photosystem II. J Am Chem Soc 119: 3415–3416

    CAS  Google Scholar 

  • Christen G and Renger G (1999) The role of hydrogen bonds for the multiphasic P680+ reduction by Yz in Photosystem II with intact oxygen evolution capacity. Analysis of kinetic H/D isotope exchange effects. Biochemistry 38: 2068–2077

    CAS  PubMed  Google Scholar 

  • Christen G, Reifarth F and Renger G (1998) On the origin of the 35 μs kinetics of P680+ reduction in Photosystem II with an intact water oxidising complex. FEBS Lett 429: 49–52

    Article  CAS  PubMed  Google Scholar 

  • Christen G, Seeliger A and Renger G (1999) P680+ reduction kinetics and redox transition probability of the water oxidizing complex as a function of pH and H D isotope exchange in spinach thylakoids. Biochemistry 38: 6082–6092

    CAS  PubMed  Google Scholar 

  • Chu H-A, Sackett H and Babcock GT (2000) Identification of a Mn-O-Mn cluster vibrational mode of the oxygen evolving complex in Photosystem II by low-frequency FTIR spectroscopy. Biochemistry 39: 14371–14376

    Article  CAS  PubMed  Google Scholar 

  • Chu HA, Hillier W, Law NA and Babcock GT (2001) Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim Biophys Acta 1503: 69–82

    CAS  PubMed  Google Scholar 

  • Chu HA, Hillier W and Debus RJ (2004) Evidence that the C-terminus of the D1 polypeptide of Photosystem II is ligated to the manganese ion that undergoes oxidation during the S1 to S2 transition: An isotope-edited FTIR study. Biochemistry 43:3152–3166

    CAS  PubMed  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. J Phys Chem B 102: 8248–8256

    Article  CAS  Google Scholar 

  • Cinco RM, Holman KLM, Robblee JH, Yano J, Pizarro SA, Bellacchio E, Sauer K and Yachandra VK (2002) Calcium EXAFS establishes the Mn-Ca cluster in the oxygen evolving complex of Photosystem II. Biochemistry 41: 12928–12933

    Article  CAS  PubMed  Google Scholar 

  • Cinco RM, Robblee JH, Messinger J, Fernandez C, Holman KLM, Sauer K and Yachandra VK (2004) Orientation of calcium in the Mn4Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of Photosystem II membranes. Biochemistry 43: 13271–13282

    CAS  PubMed  Google Scholar 

  • Clausen J and Junge W (2004) Detection of an intermediate of photosynthetic water oxidation. Nature 430: 480–483

    Article  CAS  PubMed  Google Scholar 

  • Clausen J, Debus RJ and Junge W (2004) Time-resolved oxygen production by PS II: Chasing chemical intermediates. Biochim Biophys Acta 1655: 184–194

    CAS  PubMed  Google Scholar 

  • Critchley C, Baianu IC, Govindjee and Gutowsky HS (1982) The role of chloride in O2 evolution by thylakoids from salt tolerant higher plants. Biochim Biophys Acta 682: 436–445

    CAS  Google Scholar 

  • Cua A, Stewart DH, Reifler MJ, Brudvig GW and Bocian DF (2000) Low-frequency resonance Raman characterization of the oxygen evolving complex of Photosystem II. J Am Chem Soc122:2069–2077

    Article  CAS  Google Scholar 

  • Cua A, Vrettos JS, de Paula JC, Brudvig GW and Bocian DF (2003) Raman spectra and normal coordinate analyses of low-frequency vibrations of oxo-bridged manganese complexes. J Biol Inorg Chem 8: 439–451

    CAS  PubMed  Google Scholar 

  • Dasgupta J, van Willigen RT and Dismukes GC (2004) Consequences of structural and biophysical studies for the molecular mechanism of photosynthetic oxygen evolution: Functional roles for calcium and bicarbonate. Phys Chem Chem Phys 6: 4793–4802

    CAS  Google Scholar 

  • Dau H, Andrews JC, Roelofs TA, Latimer MJ, Liang W, Yachandra VK, Sauer K and Klein MP (1995) Structural consequences of ammonia binding to the manganese cluster of the photosynthetic oxygen evolving complex: An X-ray absorption study of isotropic and oriented Photosystem II particles. Biochemistry 34:5274–5287

    Article  CAS  PubMed  Google Scholar 

  • Dau H, Iuzzolino L and Dittmer J (2001) The tetra-manganese complex of Photosystem II during its redox cycle: X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503: 24–39

    CAS  PubMed  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. Anal Bioanal Chem 376:562–583

    Article  CAS  PubMed  Google Scholar 

  • de Wijn R and van Gorkom HJ (2002) S-state dependence of the miss probability in Photosystem II. Photosynth Res 72: 217–222

    Article  PubMed  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    CAS  PubMed  Google Scholar 

  • Debus RJ (2001) Amino acid residues that modulate the properties of tyrosine Yz and the manganese cluster in the water oxidizing complex of Photosystem II. Biochim Biophys Acta 1503: 164–186

    CAS  PubMed  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. Biochim Biophys Acta 767: 176–179

    CAS  Google Scholar 

  • Delrieu MJ (1983) Evidence for unequal misses in oxygen flash yield sequence in photosynthesis. Z Naturforsch 38c: 247–258

    CAS  Google Scholar 

  • Diner BA (1977) Dependence of deactivation reactions of Photosystem II on redox state of plastoquinone pool-a varied under anaerobic conditions. Equilibria on the acceptor side of Photosystem II. Biochim Biophys Acta 460: 247–258

    CAS  PubMed  Google Scholar 

  • Diner BA (2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of Photosystem II. Proton-coupled electron transport of the redox active tyrosines and its relationship to water oxidation. Biochim Biophys Acta 1503:147–163

    CAS  PubMed  Google Scholar 

  • Diner BA and Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of Photosystem II of oxygenic photosynthesis. An Rev Plant Biol 53: 551–580

    CAS  Google Scholar 

  • Dismukes GC (1996) Manganese enzymes with binuclear active sites. Chem Rev 96: 2909–2926

    Article  CAS  PubMed  Google Scholar 

  • Dismukes GC and Siderer Y (1981) Intermediates of a polynuclear manganese cluster involved in photosynthetic oxidation of water. Proc Natl Acad Sci USA 78: 274–278

    CAS  Google Scholar 

  • Eckert HJ and Renger G (1988) Temperature dependence of P680+ reduction in O2 evolving PS II membrane fragments at different redox states Si of the water oxidizing system. FEBS Lett 236: 425–431

    Article  CAS  Google Scholar 

  • Evans MCW, Gourovskaya K and Nugent JHA (1999) Investigation of the interaction of the water oxidizing manganese complex of Photosystem II with the aqueous solvent environment. FEBS Lett 450: 285–288

    Article  CAS  PubMed  Google Scholar 

  • Evans MCW, Rich AM and Nugent JHA (2000) Evidence for the presence of a component of the Mn complex of the Photosystem II reaction centre which is exposed to water in the S2 state of the water oxidation complex. FEBS Lett 477: 113–117

    Article  CAS  PubMed  Google Scholar 

  • Evans MCW, Nugent JHA, Ball RJ, Muhiuddin I and Pace RJ (2004) Evidence for a direct manganese-oxygen ligand in water binding to the S2 state of the photosynthetic water oxidation complex. Biochemistry 43: 989–994

    CAS  PubMed  Google Scholar 

  • Fernandez C, Cinco RM, Robblee JH, Messinger J, Pizarro SA, Sauer K, Yachandra VK and Klein MP (1998) Calcium and chloride cofactors of the oxygen evolving complex: X-ray absorption spectroscopy evidence for a Mn/Ca/Cl heteronuclear cluster. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, pp 1399–1402. Kluwer Academic Publishers, Dordrecht

    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

    Article  CAS  PubMed  Google Scholar 

  • Fiege R, Zweygart W, Bittl R, Adir N, Renger G and Lubitz W (1996) EPR and ENDOR studies on the water oxidizing complex of Photosystem II. Photosynth Res 42: 227–244

    Google Scholar 

  • Fischer G and Wydrzynski T (2001) Isotope effects in FTIR difference spectra of the photosynthetic oxygen evolving catalytic site determined by ab initio calculations on model compounds. J Phys Chem B 105: 12894–12901

    CAS  Google Scholar 

  • Forbush B, Kok B and McGloin MP (1971) Cooperation of charges in photosynthetic oxygen evolution. II. Damping of flash yield oscillation, deactivation. Photochem Photobiol 14: 307–321

    CAS  Google Scholar 

  • Force DA, Randall DW, Lorigan GA, Clemens KL and Britt RD (1998) ESEEM studies of alcohol binding to the manganese cluster of the oxygen evolving complex of Photosystem II. J Am Chem Soc 120: 13321–13333

    Article  CAS  Google Scholar 

  • Förster V and Junge W (1985) Interaction of hydroxylamine with the water-oxidizing enzyme investigated via proton release. Photochem Photobiol 41: 191–194

    Google Scholar 

  • Förster V and Junge W (1986) On the action of hydroxylamine, hydrazine and their derivatives on the water oxidizing complex. Photosynth Res 9: 197–210

    Article  Google Scholar 

  • Förster V and Junge W (1988) Protolytic reactions of the photosynthetic water oxidase in the absence and in the presence of added ligands. Chem Script 28A: 111–116

    Google Scholar 

  • Frasch WD, Mei R and Sanders MA (1988) Oxidation of alcohols catalyzed by the oxygen evolving complex. Biochemistry 27: 3715–3719

    Article  CAS  Google Scholar 

  • Ghanotakis DF, Babcock GT and Yocum CF (1984) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations. FEBS Lett 167: 127–130

    Article  CAS  Google Scholar 

  • Gilchrist ML, Jr., Ball JA, Randall DW and Britt RD (1995) Proximity of the manganese cluster of Photosystem II to the redox-active tyrosine Yz. Proc Natl Acad Sci USA 92: 9545–9549

    CAS  PubMed  Google Scholar 

  • Glatzel P, Bergmann U, Yano J, Visser H, Robblee JH, Gu WW, de Groot FMF, Christou G, Pecoraro VL, Cramer SP and Yachandra VK (2004) The electronic structure of Mn in oxides, coordination complexes, and the oxygen-evolving complex of Photosystem II studied by resonant inelastic X-ray scattering. J Am Chem Soc 126: 9946–9959

    Article  CAS  PubMed  Google Scholar 

  • Gleiter HM, Haag E, Shen J-R, Eaton-Rye JJ, Seeliger AG, Inoue Y, Vermaas WFJ and Renger G (1995) Involvement of the CP47 protein in stabilization and photoactivation of a functional water oxidizing complex in the cyanobacterium Synechocystis sp PCC 6803. Biochemistry 34: 6847–6856

    Article  CAS  PubMed  Google Scholar 

  • Goussias C, Ioannidis N and Petrouleas V (1997) Low-temperature interactions of NO with the S1 and S2 states of the water oxidizing complex of Photosystem II. A novel Mn multiline EPR signal derived from the S1 state. Biochemistry 36:9261–9266

    Article  CAS  PubMed  Google Scholar 

  • Guiles RD, Zimmermann J-L, McDermott AE, Yachandra VK, Cole JL, Dexheimer SL, Britt RD, Wieghardt K, Bossek U, Sauer K and Klein MP (1990) The S3 state of Photosystem II: Differences between the structure of the manganese complex in the S2 and S3 states determined by X-ray absorption spectroscopy. Biochemistry 29: 471–485

    CAS  PubMed  Google Scholar 

  • Haddy A, Hatchell JA, Kimel RA and Thomas R (1999) Azide as a competitor of chloride in oxygen evolution by Photosystem II. Biochemistry 38: 6104–6110

    Article  CAS  PubMed  Google Scholar 

  • Hankamer B, Morris E, Nield J, Carne A and Barber J (2001) Subunit positioning and transmembrane helix organization in the core dimer of Photosystem II. FEBS Lett 504: 142–151

    Article  CAS  PubMed  Google Scholar 

  • Hansson Ö, Andréasson L-E and Vänngård T (1986) Oxygen from water is coordinated to manganese in the S2 state of Photosystem II. FEBS Lett 195: 151–154

    Article  CAS  Google Scholar 

  • Hasegawa K, Kusunoki M, Inoue Y and Ono T-A (1998) Simulation of S2-state multiline EPR signal in oriented Photosystem II membranes: Structural implications for the manganese cluster in an oxygen-evolving complex. Biochemistry 37: 9457–9465

    CAS  PubMed  Google Scholar 

  • Hasegawa K, Ono T-A, Inoue Y and Kusunoki M (1999) How to evaluate the structure of the tetranuclear Mn cluster from magnetic and EXAFS data: Case of the S2 State Mn cluster in Photosystem II. Bull Chem Soc Jpn 72: 1013–1023

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Haumann M and Junge W (1999) Photosynthetic water oxidation: A simplex scheme of its partial reactions. Biochim Biophys Acta 1411: 86–91

    CAS  PubMed  Google Scholar 

  • Haumann M and Junge W (1996) Protons and charge indicators in oxygen evolution. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 165–192. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Haumann M, Bögershausen O, Cherepanov D, Ahlbrink R and Junge W (1997) 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. Photosynth Res 51: 193–208

    Article  CAS  Google Scholar 

  • Havemann J and Mathis P (1976) Flash-induced absorption changes of the primary donor of Photosystem II at 830 nm in chloroplasts inhibited by low pH or Tris-treatment. Biochim Biophys Acta 440: 346–355

    Google Scholar 

  • Hays A-MA, Vassiliev IR, Golbeck JH and Debus RJ (1999) Role of D1-His190 in the proton coupled oxidation of tyrosine YZ in manganese depleted Photosystem II. Biochemistry 38: 11851–11865

    Article  CAS  PubMed  Google Scholar 

  • Hendry G and Wydrzynski T (2002) The two substrate water molecules are already bound to the oxygen evolving complex in the S2 state of Photosystem II. Biochemistry 41: 13328–13334

    Article  CAS  PubMed  Google Scholar 

  • Hendry G and Wydrzynski T (2003) 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in Photosystem II. Biochemistry 42: 6209–6217

    Article  CAS  PubMed  Google Scholar 

  • Hillier W and Babcock GT (2001) S-state dependent Fourier transform infrared difference spectra for the Photosystem II oxygen evolving complex. Biochemistry 40: 1503–1509

    Article  CAS  PubMed  Google Scholar 

  • Hillier W and Wydrzynski T (2000) The affinities for the two substrate water binding sites in the O2 evolving complex of Photosystem II vary independently during S-state turnover. Biochemistry 39: 4399–4405

    Article  CAS  PubMed  Google Scholar 

  • Hillier W and Wydrzynski T (2001) Oxygen ligand exchange at metal sites: Implications for the O2 evolving mechanism of Photosystem II. Biochim Biophys Acta 1503: 197–209

    CAS  PubMed  Google Scholar 

  • Hillier W and Wydrzynski T (2004) Aspects of Substrate Water Interactions within the Photosystem II Oxygen Evolving Complex. Phys Chem Chem Phys 6: 4882–4889

    Article  CAS  Google Scholar 

  • Hillier W, Messinger J and Wydrzynski T (1998) Kinetic determination of the fast exchanging substrate water molecule in the S3 state of Photosystem II. Biochemistry 37: 16908–16914

    Article  CAS  PubMed  Google Scholar 

  • Hillier W, Hendry G, Burnap RL and Wydrzynski T (2001) Substrate water exchange in Photosystem II depends on the peripheral proteins. J Biol Chem 276: 46917–46924

    Article  CAS  PubMed  Google Scholar 

  • Hind G and Whittingham CP (1963) Reduction of ferricyanide by chloroplasts in the presence of nitrogenous bases. Biochim Biophys Acta 75: 194–202

    Article  CAS  Google Scholar 

  • Hind G, Nakatani HY and Izawa S (1969) The role of Cl in photosynthesis. The Cl requirement of electron transport. Biochim Biophys Acta 172: 277–289

    CAS  PubMed  Google Scholar 

  • Hoganson CW and Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953–1956

    Article  CAS  PubMed  Google Scholar 

  • Hoganson CW, Lydakis-Simantiris N, Tang X-S, Tommos C, Warncke K, Babcock GT, Diner BA, McCracken J and Styring S (1995) A hydrogen-atom abstraction model for the function of YZ in photosynthetic oxygen evolution. Photosynth Res 46: 177–184

    Article  CAS  Google Scholar 

  • Hundelt M, Hays A-MA, 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 YZ to P680+. Biochemistry 37: 14450–14456

    Article  CAS  PubMed  Google Scholar 

  • Ioannidis N, Sarrou J, Schansker G and Petrouleas V (1998) NO reversibly reduces the water oxidizing complex of Photosystem II through S0 and S1 to the state characterized by the Mn(II)–Mn(III) multiline EPR signal. Biochemistry 37: 16445–16451

    Article  CAS  PubMed  Google Scholar 

  • Ioannidis N, Nugent JHA and Petrouleas V (2002) Intermediates of the S3 state of the oxygen evolving complex of Photosystem II. Biochemistry 41: 9589–9600

    CAS  PubMed  Google Scholar 

  • Iuzzolino L, Dittmer J, Dörner 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 S0–S1, S1–S2, and S2–S3 transitions of the water oxidation cycle. Biochemistry 37: 17112–17119

    Article  CAS  PubMed  Google Scholar 

  • Jeans C, Schilstra MJ and Klug DR (2002) The temperature dependence of P680+ reduction in oxygen evolving photosystem. Biochemistry 41: 5015–5023

    CAS  PubMed  Google Scholar 

  • Joliot P, Barbieri G and Chabaud R (1969) Un nouveau modele des centres photochimiques du systém II. Photochem Photobiol 10: 309–329

    CAS  Google Scholar 

  • Junge W, Haumann M, Ahlbrink R, Mulkidjanian A and Clausen J (2002) Electrostatics and proton transfer in photosynthetic water oxidation. Philos Trnas Roy Soc London B 357: 1407–1417

    CAS  Google Scholar 

  • Jursinic P (1981) Investigation of double turnovers in Photosystem II charge separation and oxygen evolution with excitation flashes of different duration. Biochim Biophys Acta 635: 38–52

    CAS  PubMed  Google Scholar 

  • Jursinic PA and Dennenberg RJ (1990) Oxygen release time in leaf disks and thylakoids of peas and Photosystem II membrane fragments of spinach. Biochim Biophys Acta 1020: 195–206

    CAS  Google Scholar 

  • Jursinic P and Govindjee (1977) Temperature dependence of delayed light emission in the 6 to 340 microsecond range after a single flash in chloroplasts. Photochem Photobiol 26: 617–628

    CAS  Google Scholar 

  • Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100: 98–103

    Article  CAS  PubMed  Google Scholar 

  • Karge M, Irrgang KD, Sellin S, Feinaugle R, Liu B, Eckert HJ, Eichler HJ and Renger G (1996) Effects of hydrogen deuterium exchange on photosynthetic water cleavage in PS II core complexes from spinach. FEBS Lett 378: 140–144

    Article  CAS  PubMed  Google Scholar 

  • Karge M, Irrgang K-D and Renger G (1997) Analysis of the reaction coordinate of photosynthetic water oxidation by kinetic measurements of 355 nm absorption changes at different temperatures in Photosystem II preparations suspended in either H2O or D2O. Biochemistry 36: 8904–8913

    Article  CAS  PubMed  Google Scholar 

  • Kebekus U, Messinger J and Renger G (1995) Structural changes in the water oxidizing complex monitored via the pH dependence of the reduction rate of redox state S1 by hydrazine and hydroxylamine in isolated spinach thylakoids. Biochemistry 34: 6175–6182

    Article  CAS  PubMed  Google Scholar 

  • Kelley PM and Izawa S (1978) The role of chloride ion in Photosystem II: Effects of chloride ion on Photosystem II electron transport and hydroxylamine inhibition. Biochim Biophys Acta 502: 198–210

    CAS  PubMed  Google Scholar 

  • Kimura Y and Ono TA (2001) Chelator induced disappearance of carboxylate stretching vibrational modes in S2/S1 FTIR spectrum in oxygen-evolving complex of Photosystem II. Biochemistry 40: 14061–14068

    Article  CAS  PubMed  Google Scholar 

  • Klimov VV, Allakverdiev SI, Demeter S and Krasnovsky AA (1979) Photoreduction of pheophytin in Photosystem II of chloroplasts as a function of redox potential of the medium. Dokl Akad Nauk SSSR 249: 227–230

    CAS  Google Scholar 

  • Koike H, Hanssum B, Inoue Y and Renger G (1987) Temperature dependence of the S-state transitions in a thermophilic cyanobacterium, Synschococcus vulcanus Copeland measured by absorption changes in the ultraviolet region. Biochim Biophys Acta 893: 524–533

    CAS  Google Scholar 

  • Kok B and Velthuys BR (1976) Present status of the O2 evolution model. In: Castellani A (ed) Research in Photobiology, pp 111–119. Plenum Press, New York

    Google Scholar 

  • Kok B, Forbush B and McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution. Photochem Photobiol 11: 457–476

    CAS  PubMed  Google Scholar 

  • Kretschmann H and Witt HT (1993) Chemical reduction of the water splitting enzyme system of photosynthesis and its light-induced reoxidation characterized by optical and mass spectrometric measurements: A basis for the estimation of the states of the redox active manganese and of water in the quaternary oxygen evolving S-state cycle. Biochim Biophys Acta 1144: 331–345

    CAS  Google Scholar 

  • Kretschmann H, Pauly S and Witt HT (1991) Evidence for a chemical reaction of hydroxylamine with the photosynthetic water splitting enzyme S in the dark: Possible states of manganese and water in the S-cycle. Biochim Biophys Acta 1059: 208–214

    CAS  Google Scholar 

  • Krieger A, Rutherford AW and Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor QA in Photosystem II. Biochim Biophys Acta 1229: 193–201

    Google Scholar 

  • Krishtalik LI (1986) Energetics of multielectron reactions. Photosynthetic oxygen evolution. Biochim Biophys Acta 849: 162–171

    CAS  Google Scholar 

  • Krishtalik LI (1990) Activation energy of photosynthetic oxygen evolution: An attempt at theoretical analysis. Bioelectrochem Bioenerg 23: 249–263

    Article  CAS  Google Scholar 

  • Kuzek D and Pace RJ (2001) Probing the Mn oxidation states in the OEC. Insights from spectroscopic, computational and kinetic data. Biochim Biophys Acta 1503: 123–137

    CAS  PubMed  Google Scholar 

  • Latimer MJ, DeRose VJ, Yachandra VK, Sauer K and Klein MP (1998) Structural effects of calcium depletion on the manganese cluster of Photosystem II: Determination by X-ray absorption spectroscopy. J Phys Chem B 102: 8257–8265

    Article  CAS  Google Scholar 

  • Li ZL and Burnap RL (2001) Mutations of arginine 64 within the putative Ca2+ binding lumenal interhelical a–b loop of the Photosystem II D1 protein disrupt binding of the manganese stabilizing protein and cytochrome c550 in Synechocystis sp PCC6803. Biochemistry 40: 10350–10359

    CAS  PubMed  Google Scholar 

  • Liang W, Roelofs TA, Cinco RM, Rompel A, Latimer MJ, Yu WO, Sauer K, Klein MP and Yachandra VK (2000) Structural change of the Mn cluster during the S2 to S3 state transition of the oxygen evolving complex of Photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn x-ray absorption spectroscopy. J Am Chem Soc 122: 3399–3412

    CAS  Google Scholar 

  • Limburg J, Vrettos JS, Liable-Sands LM, Rheingold AL, Crabtree RH and Brudvig GW (1999) A functional model for O-O bond formation by the O2 evolving complex in Photosystem II. Science 283: 524–527

    Article  Google Scholar 

  • Lindberg K and Andréasson L-E (1996) A one-site, two-state model for the binding of anions in Photosystem II. Biochemistry 35: 14259–14267

    Article  CAS  PubMed  Google Scholar 

  • Lindberg K, Wydrzynski T, Vänngård T and Andréasson L-E (1990) Slow release of chloride from 36Cl-labeled Photosystem II membranes. FEBS Lett 264: 153–155

    Article  CAS  Google Scholar 

  • Lindberg K, Vänngård T and Andréasson L-E (1993) Studies of the slowly exchanging chloride in Photosystem II of higher plants. Photosynth Res 38: 401–408

    Article  CAS  Google Scholar 

  • Lydakis-Simantiris N, Ghanotakis DF and Babcock GT (1997) Kinetic isotope effects on the reduction of the YZ radical in oxygen evolving and Tris washed Photosystem II membranes by time resolved EPR. Biochim Biophys Acta 1322: 129–140

    CAS  Google Scholar 

  • McEvoy JP and Brudvig GW (2004) Structure-based mechanism of photosynthetic water oxidation. Phys Chem Chem Phys 6: 4754–4763

    Article  CAS  Google Scholar 

  • McGrady JE and Stranger R (1999) Redox induced formation and cleavage of O-O σ and π bonds in a peroxo-bridged manganese dimer: a density functional study. Inorg Chem 38: 550–558

    Article  CAS  PubMed  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. Biochim Biophys Acta 1459: 481–488

    CAS  PubMed  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. Phys Chem Chem Phys 6: 4764–4771

    Article  CAS  Google Scholar 

  • Messinger J and Renger G (1994) Analysis of pH-induced modifications of the period four oscillation of the flash induced oxygen evolution reveal distinct structural changes of the Photosystem II donor side at characteristic pH values. Biochemistry 33: 10896–10905

    Article  CAS  PubMed  Google Scholar 

  • Messinger J, Wacker U and Renger G (1991) Unusual low reactivity of the water oxidase in the redox state S3 toward exogenous reductants. Analysis of the NH2OH and NH2NH2 induced modifications of flash induced oxygen evolution in isolated spinach thylakoids. Biochemistry 30: 7852–7862

    Article  CAS  PubMed  Google Scholar 

  • Messinger J, Schröder WP and Renger G (1993) Structure-function relations in Photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash induced oxygen evolution. Biochemistry 32: 7658–7668

    CAS  PubMed  Google Scholar 

  • Messinger J, Badger M and Wydrzynski T (1995) Detection of one slowly exchanging substrate water molecule in the S3 state of Photosystem II. Proc Natl Acad Sci USA 92: 3209–3213

    CAS  PubMed  Google Scholar 

  • Messinger J, Nugent JHA and Evans MCW (1997a) Detection of an EPR multiline signal for the S *0 state in Photosystem II. Biochemistry 36: 11055–11060

    CAS  PubMed  Google Scholar 

  • Messinger J, Seaton G, Wydrzynski T, Wacker U and Renger G (1997b) S−3 state of the water oxidase in Photosystem II. Biochemistry 36: 6862–6873

    CAS  PubMed  Google Scholar 

  • Messinger J, Robblee JH, Yu WO, Sauer K, Yachandra VK and Klein MP (1997c) The S0 state of the oxygen evolving complex in Photosystem II is paramagnetic: detection of an EPR multiline signal. J Am Chem Soc 119: 11349–11350

    Article  CAS  Google Scholar 

  • Messinger J, Robblee JH, Fernandez C, Cinco RM, Visser H, Bergmann U, Glatzel P, Cramer SP, Campbell KA, Peloquin JM, Britt RD, Sauer K, Klein MP and Yachandra VK (1998) Oxidation states and structure of the manganese cluster in the S0 State of the oxygen evolving complex. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, pp 1279–1282. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Messinger J, Robblee J, Bergmann U, Fernandez C, Glatzel P, Isgandarova S, Hanssum B, Renger G, Cramer S, Sauer K and Yachandra V (2001a) Manganese oxidation states in Photosystem II. In: PS2001: Proceedings of the 12th International Congress on Photosynthesis, S10-019. CSIRO Publishing, Melbourne (CD-RO)

    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 (2001b) Absence of Mn centered oxidation in the S2 to S3 transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc 123: 7804–7820

    Article  CAS  PubMed  Google Scholar 

  • Metz JG, Nixon PJ, Rögner M, Brudvig GW and Diner BA (1989) Directed alteration of the D1 polypeptide of Photosystem II: Evidence that tyrosine-161 is the redox component, Z, connecting the oxygen evolving complex to the primary electron donor, P680. Biochemistry 28: 6960–6969

    Article  CAS  PubMed  Google Scholar 

  • Meunier PC and Popovic R (1991) The time for oxygen release in photosynthesis: Reconciliation of flash polarography with other measurement techniques. Photosynth Res 28: 33–39

    Article  CAS  Google Scholar 

  • Meyer B, Schlodder E, Dekker JP and Witt HT (1989) O2 evolution and Chl a II+ (P680+) nanosecond reduction kinetics in single flashes as a function of pH. Biochim Biophys Acta 974: 36–43

    CAS  Google Scholar 

  • Miyao M, Murata N, Lavorel J, Maisonpeteri B, Boussac A and Etienne AL (1987) Effect of the 33-kDa protein on the S-state transitions in photosynthetic oxygen evolution. Biochim Biophys Acta 890: 151–159

    CAS  Google Scholar 

  • Noguchi T and Sugiura M (2000) Structure of an active water molecule in the water oxidizing complex of Photosy stem II as studied by FTIR spectroscopy. Biochemistry 39: 10943–10949

    Article  CAS  PubMed  Google Scholar 

  • Noguchi T and Sugiura M (2001) Flash induced Fourier transform infrared detection of the structural changes during the S-state cycle of the oxygen evolving complex in Photosystem II. Biochemistry 40: 1497–1502

    CAS  PubMed  Google Scholar 

  • Noguchi T and Sugiura M (2002a) Flash-induced FTIR difference spectra of the water oxidizing complex in moderately hydrated Photosystem II core films: Effect of hydration extent on S-state transitions. Biochemistry 41: 2322–2330

    CAS  PubMed  Google Scholar 

  • Noguchi T and Sugiura M (2002b) FTIR detection of water reactions during the flash-induced S-state cycle of the photosynthetic water oxidizing complex. Biochemistry 41: 15706–15712

    CAS  PubMed  Google Scholar 

  • Noguchi T, Ono T-A and Inoue Y (1995a) Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygen evolving center by means of Fourier transform infrared spectroscopy. Biochim Biophys Acta 1228: 189–200

    Google Scholar 

  • Noguchi T, Ono T-A and Inoue Y (1995b) A carboxylate ligand interacting with water in the oxygen evolving center of Photosystem II as revealed by Fourier transform infrared spectroscopy. Biochim Biophys Acta 1232: 59–66

    Google Scholar 

  • Nugent JHA, Demetriou C and Lockett CJ (1987) Electron donation in Photosystem II. Biochim Biophys Acta 894: 534–542

    CAS  Google Scholar 

  • Nugent JHA, Rich AM and Evans MCW (2001) Photosynthetic water oxidation: Towards a mechanism. Biochim Biophys Acta 1503: 138–146

    CAS  PubMed  Google Scholar 

  • Nugent JHA, Muhiuddin IP and Evans MCW (2002) Electron transfer from the water oxidizing complex at cryogenic temperatures: The S1 to S2 step. Biochemistry 41: 4117–4126

    Article  CAS  PubMed  Google Scholar 

  • Olesen K and Andréasson L-E (2003) The function of the chloride ion in photosynthetic oxygen evolution. Biochemistry 42: 2025–2035

    Article  CAS  PubMed  Google Scholar 

  • Ono T-A (2001) Metallo-radical hypothesis for photoassembly of Mn4 cluster of photosynthetic oxygen evolving complex. Biochim Biophys Acta 1503: 40–51

    CAS  PubMed  Google Scholar 

  • Ono T-A, Zimmermann J-L, Inoue Y and Rutherford AW (1986) EPR evidence for a modified S-state transition in chloride depleted Photosystem II. Biochim Biophys Acta 851: 193–201

    CAS  Google Scholar 

  • Ono T-A, Noguchi T, Inoue Y, Kusunoki M, Yamaguchi H and Oyanagi H (1995) XANES spectroscopy for monitoring intermediate reaction states of Cl depleted Mn cluster in photosynthetic water oxidation enzyme. J Am Chem Soc 117: 6386–6387

    Article  CAS  Google Scholar 

  • Pace RJ, Smith P, Bramley R and Stehlik D (1991) EPR saturation and temperature dependence studies on signals from the oxygen evolving center of Photosystem II. Biochim Biophys Acta 1058: 161–170

    CAS  Google Scholar 

  • Page CC, Moser CC, Chen XX and Dutton PL (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402: 47–52

    CAS  PubMed  Google Scholar 

  • Pecoraro VL (ed) (1992) Manganese Redox Enzymes. VCH Publishers, New York

    Google Scholar 

  • Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh W-Y and Law NA (1998) A proposal for water oxidation in Photosystem II. Pure Appl Chem 70: 925–929

    CAS  Google Scholar 

  • Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WH and Britt RD (2000) 55Mn ENDOR of the S2-State Multiline EPR Signal of Photosystem II: Implications on the Structure of the Tetranuclear Mn Cluster. J Am Chem Soc 122: 10926–10942

    Article  CAS  Google Scholar 

  • Penner-Hahn JE (1998) Structural characterization of the Mn site in the photosynthetic oxygen evolving complex. Struct Bond 90: 1–36

    CAS  Google Scholar 

  • Putnam-Evans C, Burnap R, Wu J, Whitmarsh J and Bricker TM (1996) Site directed mutagenesis of the CP 47 protein of Photosystem II: Alteration of conserved charged residues in the domain 364E–444R. Biochemistry 35: 4046–4053

    Article  CAS  PubMed  Google Scholar 

  • Qian M, Dao L, Debus RJ and Burnap RL (1999) Impact of mutations within the putative Ca2+-binding lumenal Interhelical a–b loop of the Photosystem II D1 protein on the kinetics of photoactivation and H2O oxidation in Synechocystis sp. PCC6803. Biochemistry 38: 6070–6081

    Article  CAS  PubMed  Google Scholar 

  • Radmer R and Ollinger O (1983) Topography of the O2 evolving site determined with water analogs. FEBS Letter 152: 39–43

    Article  CAS  Google Scholar 

  • Radmer R and Ollinger O (1986) Do the higher oxidation states of the photosynthetic O2 evolving system contain bound water? FEBS Lett 195: 285–289

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F and Lavergne J (1991) Proton release during successive oxidation steps of the photosynthetic water oxidation process — Stoichiometries and pH-dependence. Biochemistry 30: 10004–10012

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F and Lavergne J (2001) Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim Biophys Acta 1503: 246–259

    CAS  PubMed  Google Scholar 

  • Rappaport F, Blanchard-Desce M and Lavergne J (1994) Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen evolving complex. Biochim Biophys Acta 1184: 178–192

    CAS  Google Scholar 

  • Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA and Lavergne J (2002) Kinetics and pathways of charge recombination in Photosystem II. Biochemistry 41: 8518–8527

    Article  CAS  PubMed  Google Scholar 

  • Rashid A and Homann PH (1992) Properties of iodide activated photosynthetic water oxidizing complexes. Biochim Biophys Acta 1101: 303–310

    CAS  Google Scholar 

  • Razeghifard MR and Pace RJ (1999) EPR kinetic studies of oxygen release in thylakoids in PS II membranes: a kinetic intermediate in the S3 to S0 transition. Biochemistry 38: 1252–1257

    Article  CAS  PubMed  Google Scholar 

  • Razeghifard MR, Klughammer C and Pace RJ (1997a) Electron paramagnetic resonance kinetic studies of the S states in spinach thylakoids. Biochemistry 36: 86–92

    CAS  PubMed  Google Scholar 

  • Razeghifard MR, Wydrzynski T, Pace RJ and Burnap RL (1997b) Y Z reduction kinetics in the absence of the manganese stabilizing protein of Photosystem II. Biochemistry 36: 14474–14478

    CAS  PubMed  Google Scholar 

  • Renger G (1987) Mechanistic aspects of photosynthetic water cleavage. Photosynthetica 21: 203–224

    CAS  Google Scholar 

  • Renger G (1997) Mechanistic and structural aspects of photosynthetic water oxidation. Physiol Plant 100: 828–841

    Article  CAS  Google Scholar 

  • Renger G (2001) Photosynthetic water oxidation to molecular oxygen: Apparatus and mechanism. Biochim Biophys Acta 1503: 210–228

    CAS  PubMed  Google Scholar 

  • Renger G (1999) Mechanism of photosynthetic water cleavage. In: Singhal GS, Renger G, Sopory SK, Irrgang K-D and Govindjee (eds) Concepts in Photobiology: Photosynthesis and Photomorphogenesis, pp 292–329. Narosa Publishing House, New Delhi, India

    Google Scholar 

  • Renger G and Hanssum B (1988) Studies on the deconvolution of flash induced absorption changes into the difference spectra of individual redox steps within the water oxidizing enzyme system. Photosynth Res 16: 243–259

    Article  CAS  Google Scholar 

  • Renger G and Hanssum B (1992) Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett 299: 28–32

    Article  CAS  PubMed  Google Scholar 

  • Renger G and Weiss W (1986) Functional and structural aspects of photosynthetic water oxidation. Biochem Soc Trans 14: 17–20

    CAS  PubMed  Google Scholar 

  • Renger G and Wolff C (1976) The existence of a high photochemical turnover rate at the reaction centers of system II in Triswashed chloroplasts. Biochim Biophys Acta 423: 610–614

    CAS  PubMed  Google Scholar 

  • Renger G, Christen G, Karge M, Eckert H-J and Irrgang K-D (1998) Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation: results and implications. J Bioinorg Chem 3: 360–366

    CAS  Google Scholar 

  • Rich PR (1996) Electron transfer complexes coupled to ion translocation. In: Bendall DS (ed) Protein Electron Transfer, pp 217–248. BIOS Scientific Publishers, Oxford

    Google Scholar 

  • Richens DT (1997) The Chemistry of Aqua Ions. John Wiley & Sons, Chichester

    Google Scholar 

  • Riggs PJ, Mei R, Yocum CF and Penner-Hahn JE (1992) Reduced derivatives of the manganese cluster in the photosynthetic oxygen evolving complex. J Am Chem Soc 114: 10650–10651

    CAS  Google Scholar 

  • Riggs-Gelasco PJ, Mei R, Yocum CF and Penner-Hahn JE (1996) Reduced derivatives of the Mn cluster in the oxygen evolving complex of Photosystem II: an EXAFS study. J Am Chem Soc 118: 2387–2399

    CAS  Google Scholar 

  • Robblee JH, Cinco RM and Yachandra VK (2001) X-ray spectroscopy based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta 1503: 7–23

    CAS  PubMed  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 S0 state of the oxygen evolving complex of Photosystem II studied by EXAFS spectroscopy: Are there three di-μ-oxo-bridged Mn2 moieties in the tetranuclear Mn complex? J Am Chem Soc 124: 7459–7471

    Article  CAS  PubMed  Google Scholar 

  • Robinson HH and Crofts AR (1983) Kinetics of the oxidation reduction reactions of the Photosystem II quinone acceptor complex, and the pathway for deactivation. FEBS Lett 153: 221–226

    Article  CAS  Google Scholar 

  • Robinson HH, Sharp RR and Yocum CF (1981) On the origin of light induced changes in the proton magnetic relaxation rate of chloroplast thylakoid membrane suspensions. Arch Biochem Biophys 207: 1–8

    Article  CAS  PubMed  Google Scholar 

  • Roelofs TA, Liang W, Latimer MJ, Cinco RM, Rompel A, Andrews JC, Sauer K, Yachandra VK and Klein MP (1996) Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen evolving complex. Proc Natl Acad Sci USA 93: 3335–3340

    Article  CAS  PubMed  Google Scholar 

  • Rutherford AW and Inoue Y (1984) Oscillation of delayed luminescence from PS II: Recombination of S2QB and S3QB. FEBS Lett 165: 163–170

    CAS  Google Scholar 

  • Rutherford AW and Styring S (1987) EPR signal II in Photosystem II: Redox and paramagnetic interactions with the molecular oxygen evolving enzyme. Cytochrome Syst: Mol Biol Bioenerg, [Proc UNESCO Int Symp]: 541–547

    Google Scholar 

  • Rutherford AW, Crofts AR and Inoue Y (1982) Thermoluminescence as a probe of Photosystem II photochemistry. The origin of the flash-induced glow peaks. Biochim Biophys Acta 682: 457–465

    CAS  Google Scholar 

  • Sandusky PO and Yocum CF (1984) The chloride requirement for photosynthetic oxygen evolution: analysis of the effects of chloride and other anions on amine inhibition of the oxygen evolving complex. Biochim Biophys Acta 766: 603–611

    CAS  Google Scholar 

  • Sandusky PO and Yocum CF(1986) The chloride requirement for photosynthetic oxygen evolution: Factors affecting nucleophilic displacement of chloride from the oxygen evolving complex. Biochim Biophys Acta 849: 85–93

    CAS  Google Scholar 

  • Sarrou J, Ioannidis N, Deligiannakis Y and Petrouleas V (1998) A Mn(II)–Mn(III) EPR signal arises from the interaction of NO with the S1 state of the water oxidizing complex of Photosystem II. Biochemistry 37: 3581–3587

    Article  CAS  PubMed  Google Scholar 

  • Sarrou J, Isgandarova S, Kern J, Zouni A, Renger G, Lubitz W and Messinger J (2003) Nitric Oxide induced formation of the S−2 state in the oxygen evolving complex of Photosystem II from Synechococcus elongatus. Biochemistry 42: 1016–1023

    Article  CAS  PubMed  Google Scholar 

  • Sauer K and Yachandra VK (2002) A possible evolutionary origin for the Mn4 cluster of the photosynthetic water oxidation complex from natural MnO2 precipitates in the early ocean. Proc Natl Acad Sci USA 99: 8631–8636

    Article  CAS  PubMed  Google Scholar 

  • Saygin O and Witt HT (1985) Sequence of the redox changes of manganese and pattern of the changes of charges during water cleavage in photosynthesis. Optical events in the UV and the red region in the presence and absence of hydroxylamine. Photobiochem Photobiophys 10: 71–82

    CAS  Google Scholar 

  • Schansker G, Goussias C, Petrouleas V and Rutherford AW (2002) Reduction of the Mn cluster of the water oxidizing enzyme by nitric oxide: formation of an S−2 state. Biochemistry 41: 3057–3064

    Article  CAS  PubMed  Google Scholar 

  • Schilstra MJ, Rappaport F, Nugent JHA, Barnett CJ and Klug DR (1998) Proton/hydrogen transfer affects the S-state dependent microsecond phases of P680+ reduction during water splitting. Biochemistry 37: 3974–3981

    Article  CAS  PubMed  Google Scholar 

  • Schlodder E and Witt HT (1999) Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation. J Biol Chem 274: 30387–30392

    Article  CAS  PubMed  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of Photosystem II. Biochim Biophys Acta 1277: 35–60

    PubMed  Google Scholar 

  • Sharp PR (1992) Proton NMR relaxation due to photosynthetic oxygen evolving center. In: Pecoraro VL (ed) Manganese Redox Enzymes, pp 177–196. VCH Publishers, New York

    Google Scholar 

  • Shen J-R, Ikeuchi M and Inoue Y (1992) Stoichiometric association of extrinsic cytochrome c550 and 12 kDa protein with a highly purified oxygen evolving Photosystem II core complex from Synechococcus vulcanus. FEBS Lett 301: 145–149

    Article  CAS  PubMed  Google Scholar 

  • Shi LX and Schroder WP (2004) The low molecular mass subunits of the photosynthetic supracomplex, Photosystem II. Biochim Biophys Acta 1608: 75–96

    CAS  PubMed  Google Scholar 

  • Shinkarev VP (1996) Binary oscillations in the Kok model of oxygen evolution in oxygenic photosynthesis. Photosynth Res 48: 411–417

    Article  CAS  Google Scholar 

  • Shinkarev V and Wraight CA (1993) Oxygen evolution in photosynthesis: From unicycle to bicycle. Proc Natl Acad Sci USA 90: 1834–1838

    CAS  PubMed  Google Scholar 

  • Siegbahn PEM (2000) Theoretical models for the oxygen radical mechanism of water oxidation and the water oxidizing complex of Photosystem II. Inorg Chem 39: 2923–2935

    Article  CAS  PubMed  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. J Am Chem Soc 121: 117–127

    Article  CAS  Google Scholar 

  • Sigel A and Sigel H (2000) Manganese and Its Role in Biological Processes. Marcel Dekker, Inc, New York

    Google Scholar 

  • Sinclair J and Arnason T (1974) Studies on a thermal reaction associated with photosynthetic oxygen evolution. Biochim Biophys Acta 368: 393–400

    CAS  PubMed  Google Scholar 

  • Sivaraja M, Hunziker D and Dismukes GC (1988) The reaction of hydrogen sulfide with the photosynthetic water oxidizing complex and its lack of reaction with the primary electron acceptor in spinach. Biochim Biophys Acta 936: 228–235

    CAS  Google Scholar 

  • Strzalka K, Walczak T, Sarna T and Swartz HM (1990) Measurement of time-resolved oxygen concentration changes in photosynthetic systems by nitroxide-based EPR oximetry. Arch Biochem Biophys 281: 312–318

    Article  CAS  PubMed  Google Scholar 

  • Styring S and Rutherford AW (1987) In the oxygen evolving complex of Photosystem II the S0 state is oxidized to the S1 state by YD+ (Signal IIslow). Biochemistry 26: 2401–2405

    Article  CAS  Google Scholar 

  • Styring S and Rutherford AW (1988) Deactivation kinetics and temperature dependence of the S-state transitions in the oxygen evolving system of Photosystem II measured by EPR spectroscopy. Biochim Biophys Acta 933: 378–387

    CAS  Google Scholar 

  • Tamura N and Cheniae G (1987) Photoactivation of the water-oxidizing complex in Photosystem II membranes depleted of Mn and extrinsic proteins. I. Biochemical and kinetic characterization. Biochim Biophys Acta 890: 179–194

    CAS  Google Scholar 

  • Tamura N, Inoue Y and Cheniae GM (1989) Photoactivation of the water oxidizing complex in Photosystem II membranes depleted of Mn, Ca and extrinsic proteins. II. Studies on the functions of Ca2+. Biochim Biophys Acta 976: 173–181

    CAS  Google Scholar 

  • Tang XS, Zheng M, Chisholm DA, Dismukes GC and Diner BA (1996) Investigation of the differences in the local protein environments surrounding tyrosine radicals Y Z and Y D in Photosystem II using wild type and the D2-Tyr160Phe mutant of Synechocystis 6803. Biochemistry 35: 1475–1484

    CAS  PubMed  Google Scholar 

  • Tommos C (2002) Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation. Philos Trans Roy Soc London B 357: 1383–1394

    CAS  Google Scholar 

  • Tommos C and Babcock GT (1998) Oxygen production in nature: A light-driven metalloradical enzyme process. Acc Chem Res 31: 18–25

    Article  CAS  Google Scholar 

  • Tommos C and Babcock GT (2000) Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta 1458: 199–219

    CAS  PubMed  Google Scholar 

  • Tommos C, Tang XS, Warncke K, Hoganson CW, Styring S, McCracken J, Diner BA and Babcock GT (1995) Spin-density distribution, conformation, and hydrogen bonding of the redox active tyrosine YZ in Photosystem II from multiple electron magnetic resonance spectroscopies: implications for photosynthetic oxygen evolution. J Am Chem Soc 117: 10325–10335

    Article  CAS  Google Scholar 

  • Tommos C, Hoganson CW, Di Valentin M, Lydakis-Simantiris N, Dorlet P, Westphal K, Chu H-A, McCracken J and Babcock GT (1998) Manganese and tyrosyl radical function in photosynthetic oxygen evolution. Curr Op Chem Biol 2: 244–252

    CAS  Google Scholar 

  • van Gorkom HJ and Gast P (1996) Measurement of photosynthetic oxygen evolution. In: Amesz J and Hoff AJ (eds) Biophysical Techniques in Photosynthesis, pp 391–405. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • van Leeuwen PJ, Hermann C and van Gorkom HJ (1993) Absorbance difference spectra of the S-state transitions in Photosystem II core particles. Photosynth Res 38: 323–330

    Google Scholar 

  • van Rensen JJS, Xu C and Govindjee (1999) Role of bicarbonate in Photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis. Physiol Plant 105: 585–592

    Google Scholar 

  • van Vliet P and Rutherford AW (1996) Properties of the chloride depleted oxygen evolving complex of Photosystem II studied by electron paramagnetic resonance. Biochemistry 35: 1829–1839

    PubMed  Google Scholar 

  • van Vliet P, Boussac A and Rutherford AW (1994) Chloride depletion effects in the calcium deficient oxygen evolving complex of Photosystem II. Biochemistry 33: 12998–13004

    PubMed  Google Scholar 

  • Vass I and Styring S (1991) pH dependent charge equilibria between tyrosine-D and the S-states in Photosystem II. Estimation of relative midpoint potentials. Biochemistry 30: 830–839

    Article  CAS  PubMed  Google Scholar 

  • Vass I, Deak Z and Hideg E (1990) Charge equilibrium between the water oxidizing complex and the electron donor tyrosine D in Photosystem II. Biochim Biophys Acta 1017: 63–69

    CAS  Google Scholar 

  • Velthuys B and Kok B (1978) Photosynthetic oxygen evolution from hydrogen peroxide. Biochim Biophys Acta 502: 211–221

    CAS  PubMed  Google Scholar 

  • Vermaas WEJ, Renger G and Dohnt G (1984) The reduction of the oxygen evolving system in chloroplasts by thylakoid components. Biochim Biophys Acta 764: 194–202

    CAS  Google Scholar 

  • Vermaas WFJ, Rutherford AW and Hansson O (1988) Site directed mutagenesis in Photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: Donor D is a tyrosine residue in the D2 protein. Proc Natl Acad Sci USA 85: 8477–8481

    CAS  Google Scholar 

  • Visser H, Anxolabéhère-Mallart E, Bergmann U, Glatzel P, Robblee JH, Cramer SP, Girerd J-J, Sauer K, Klein MP and Yachandra VK (2001) Mn K-edge XANES and Kβ XES studies of two Mn-Oxo Binuclear complexes: Investigation of three different oxidation states relevant to the oxygen-evolving complex of Photosystem II. J Am Chem Soc 123: 7031–7039

    Article  CAS  PubMed  Google Scholar 

  • Volkov AG (1989) Oxygen evolution in the course of photosynthesis: Molecular mechanisms. Bioelectrochem Bioenerg 21: 3–24

    Article  CAS  Google Scholar 

  • Vos MH, van Gorkom HJ and van Leeuwen PJ (1991) An electroluminescence study of stabilization reactions in the oxygen evolving complex of Photosystem II. Biochim Biophys Acta 1056: 27–39

    CAS  Google Scholar 

  • Vrettos JS, Limburg J and Brudvig GW (2001a) Mechanism of photosynthetic water oxidation: Combining biophysical studies of Photosystem II with inorganic model chemistry. Biochim Biophys Acta 1503: 229–245

    CAS  PubMed  Google Scholar 

  • Vrettos JS, Stone DA and Brudvig GW (2001b) Quantifying the ion selectivity of the Ca2+ site in Photosystem II: evidence for direct involvement of Ca2+ in O2 formation. Biochemistry 40: 7937–7945

    Article  CAS  PubMed  Google Scholar 

  • Weng TC, Hsieh WY, Uffelman ES, Gordon-Wylie SW, Collins TJ, Pecoraro VL and Penner-Hahn JE (2004) XANES evidence against a manganyl species in the S3 state of the oxygen-evolving complex. J Am Chem Soc 126: 8070–8071

    Article  CAS  PubMed  Google Scholar 

  • Westphal KL, Lydakis-Simantiris N, Cukier RI and Babcock GT (2000) Effects of Sr2+ substitution on the reduction rates of Y Z in PS II membranes: Evidence for concerted hydrogen atom transfer in oxygen evolution. Biochemistry 39: 16220–16229

    Article  CAS  PubMed  Google Scholar 

  • Wieghardt K (1989) The active sites in manganese containing metalloproteins and inorganic model complexes. Angew Chem Int Ed Engl 28: 1153–1172

    Article  Google Scholar 

  • Wincencjusz H, Yocum CF and van Gorkom HJ (1998) S-state dependence of chloride binding affinities and exchange dynamics in the intact and polypeptide-depleted O2 evolving complex of Photosystem II. Biochemistry 37: 8595–8604

    Article  CAS  PubMed  Google Scholar 

  • Wincencjusz H, Yocum CF and van Gorkom HJ (1999) Activating anions that replace Cl in the O2 evolving complex of Photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states. Biochemistry 38: 3719–3725

    Article  CAS  PubMed  Google Scholar 

  • Witt HT (1996) Primary reactions of oxygenic photosynthesis. Ber Bunsenges Phys Chem 100: 1923–1942

    CAS  Google Scholar 

  • Wydrzynski T and Renger G (1986) On the interpretation of the NMR water-proton relaxivity of photosynthetic membrane samples: Ramifications in the use of EDTA. Biochim Biophys Acta 851: 65–74

    CAS  Google Scholar 

  • Wydrzynski T, Zumbulyadis N, Schmidt PG, Gutowsky HS and Govindjee (1976) Proton relaxation and charge accumulation during oxygen evolution in photosynthesis. Proc Natl Acad Sci USA 73: 1196–1198.

    CAS  Google Scholar 

  • Wydrzynski T, Hillier W and Messinger J (1996) On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism. Physiol Plant 96: 342–350

    Article  CAS  Google Scholar 

  • Yachandra VK (2002) Structure of the manganese complex in Photosystem II: Insights from X-ray spectroscopy. Philos T Roy Soc B 357: 1347–1358

    CAS  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

    CAS  PubMed  Google Scholar 

  • Yachandra VK, Sauer K and Klein MP (1996) Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen. Chem Rev 96: 2927–2950

    Article  CAS  PubMed  Google Scholar 

  • Yamanari T, Kimura Y, Mizusawa N, Ishii A and Ono T-A (2004) Mid-to low-frequency Fourier transform infrared spectra of the S-state cycle for photosynthetic water oxidation in Synechocystis sp. PCC 6803. Biochemistry 43: 7479–7490

    Article  CAS  PubMed  Google Scholar 

  • Yocum CF (1992) The calcium and chloride requirements for photosynthetic water oxidation. In: Pecoraro VL (ed) Manganese Redox Enzymes, pp 71–84. VCH Publishers, New York

    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. Inorg Chem 35: 3307–3319

    CAS  PubMed  Google Scholar 

  • Zheng M, Khangulov SV, Dismukes GC and Barynin VV (1994) Electronic structure of dimanganese(II,III) and dimanganese(III,IV) complexes and dimanganese catalase enzyme: A general EPR spectral simulation approach. Inorg Chem 33: 382–387

    Article  CAS  Google Scholar 

  • Zimmermann J-L and Rutherford AW (1986) Electron paramagnetic resonance properties of the S2 state of the oxygen-evolving complex of Photosystem II. Biochemistry 25: 4609–4615

    Article  CAS  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 Å resolution. Nature 409: 739–743

    Article  CAS  PubMed  Google Scholar 

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Hillier, W., Messinger, J. (2005). Mechanism of Photosynthetic Oxygen Production. In: Wydrzynski, T.J., Satoh, K., Freeman, J.A. (eds) Photosystem II. Advances in Photosynthesis and Respiration, vol 22. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4254-X_26

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