Eight steps preceding O-O bond formation in oxygenic photosynthesis-A basic reaction cycle of the Photosystem II manganese complex

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1767, Issue 6, 2007, Pages 472-483

  Dau, Holger ^a   Haumann, Michael ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Kok cycle; Manganese complex; Oxygen evolution; Photosynthesis; Proton release; Water oxidation

Indexed keywords

MANGANESE; OXYGEN;

BINDING KINETICS; COMPLEX FORMATION; ELECTRON TRANSPORT; NONHUMAN; OXIDATION KINETICS; OXYGEN TRANSPORT; PHASE TRANSITION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM CHEMISTRY; REACTION ANALYSIS; REVIEW; WATER ANALYSIS;

ELECTRONS; KINETICS; MANGANESE; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTONS; WATER;

CYANOBACTERIA;

EID: 34249847311     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2007.02.022     Document Type: Review

References (114)

1. Blankenship R.E. Molecular Mechanisms of Photosynthesis (2002), Blackwell Science
2. Nugent J.H.A. Photosynthetic Water oxidation (special issue). Biochim. Biophys. Acta 1503 (2001) 1-259
3. Debus R.J. The manganese and calcium ions of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1102 (1992) 269-352
4. Ort D., and Yocum C.F. Oxygenic Photosynthesis-The Light Reactions vol. 10 (1996), Kluwer Academic Publ, Dordrecht
5. Diner B.A., and Rappaport F. Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu. Rev. Plant Biol. 53 (2002) 551-580
6. Barber J. PhotosystemII: the engine of life. Quart. Rev. Biophys. 36 (2003) 71-89
7. McEvoy J.P., and Brudvig G.W. Water-splitting chemistry of Photosystem II. Chem. Rev. 106 (2006) 4455-4483
8. 2 formation tracked by time-resolved X-ray experiments. Science 310 (2005) 1019-1021
9. Zouni A., Witt H.T., Kern J., Fromme P., Krauss N., Saenger W., and Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409 (2001) 739-743
10. Kamiya N., and Shen J.-R. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 98-103
11. Ferreira K.N., Iverson T.M., Maghlaoui K., Barber J., and Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science 303 (2004) 1831-1838
12. Loll B., Kern J., Saenger W., Zouni A., and Biesiadka J. Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438 (2005) 1040-1044
13. Kern J., Loll B., Zouni A., Saenger W., Irrgang K.D., and Biesiadka J. Cyanobacterial photosystem II at 3.2 A resolution-the plastoquinone binding pockets. Photosynth. Res. 84 (2005) 153-159
14. Hankamer B., Morris E.P., and Barber J. Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography. Nat. Struct. Biol. 6 (1999) 560-564
15. Nield J., Orlova E.V., Morris E.P., Gowen B., van Heel M., and Barber J. 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat. Struct. Biol. 7 (2000) 44-47
16. Rhee K.H., Morris E.P., Barber J., and Kuhlbrandt W. Three-dimensional structure of the plant photosystem II reaction centre at 8 A resolution. Nature 396 (1998) 283-286
17. Morris E.P., Hankamer B., Zheleva D., Friso G., and Barber J. The three-dimensional structure of a photosystem II core complex determined by electron crystallography. Structure 5 (1997) 837-849
18. Dau H., Liebisch P., and Haumann M. The structure of the manganese complex of photosystem II in its dark-stable S1-state: EXAFS results in relation to recent crystallographic data. Phys. Chem. Chem. Phys. 6 (2004) 4781-4792
19. Yano J., Kern J., Irrgang K.-D., Latimer M.J., Bergmann U., Glatzel P., Pushkar Y., Biesiadka J., Loll B., Sauer K., Messinger J., Zouni A., and Yachandra V.K. X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 12047-12052
20. Grabolle M., Haumann M., Muller C., Liebisch P., and Dau H. Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K. J. Biol. Chem. 281 (2006) 4580-4588
21. Dau H., Iuzzolino L., and Dittmer J. The tetra-manganese complex of photosystem II during its redox cycle: X-ray absorption results and mechanistic implications. Biochim. Biophys. Acta 1503 (2001) 24-39
22. Robblee J.H., Cinco R.M., and Yachandra V.K. X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1503 (2001) 7-23
23. Dau H., Liebisch P., and Haumann M. 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 (2003) 562-583
24. Yachandra V.K. In: Sauer K. (Ed). Methods in enzymology-Biochemical spectroscopy (1995), Academic Press, New York 638-678
25. Dau H., and Haumann M. X-ray absorption spectroscopy to watch catalysis by metalloenzymes: status and perspectives discussed for the water-splitting manganese complex of photosynthesis. J. Synchrotron Radiat. 10 (2003) 76-85
26. Penner-Hahn J.E. In: Hill H.A.O., Sadler P.J., and Thomson A.J. (Eds). Metal sites in proteins and Models: Redox centres (1999), Springer, Berlin 1-36
27. Debus R.J. Amino acid residues that modulate the properties of tyrosine Y(Z) and the manganese cluster in the water oxidizing complex of photosystem II. Biochim. Biophys. Acta 1503 (2001) 164-186
28. Chu H.A., Hillier W., Law N.A., and Babcock G.T. Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim. Biophys. Acta 1503 (2001) 69-82
29. Yamanari T., Kimura Y., Mizusawa N., Ishii A., and Ono T.-a. Mid- to Low-Frequency Fourier Transform Infrared Spectra of S-State Cycle for Photosynthetic Water Oxidation in Synechocystis sp. PCC 6803. Biochemistry 43 (2004) 7479-7490
30. Berthomieu C., and Hienerwadel R. Vibrational spectroscopy to study the properties of redox-active tyrosines in photosystem II and other proteins. Biochim. Biophys. Acta 1707 (2005) 51-66
31. Noguchi T., and Sugiura M. Structure of an active water molecule in the water-oxidizing complex of photosystem II as studied by FTIR spectroscopy. Biochemistry 39 (2000) 10943-10949
32. Peloquin J.M., and Britt R.D. EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim. Biophys. Acta 1503 (2001) 96-111
33. Carrell G., Tyryshkin M., and Dismukes C. An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J. Biol. Inorg. Chem. 7 (2002) 2-22
34. Britt R.D., Campbell K.A., Peloquin J.M., Gilchrist M.L., Aznar C.P., Dicus M.M., Robblee J., and Messinger J. Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta 1655 (2004) 158-171
35. Geijer P., Peterson S., Ahrling K.A., Deak Z., and Styring S. Comparative studies of the S0 and S2 multiline electron paramagnetic resonance signals from the manganese cluster in Photosystem II. Biochim. Biophys. Acta 1503 (2001) 83-95
36. Koulougliotis D., Shen J.-R., Ioannidis N., and Petrouleas V. Near-IR irradiation of the S2 state of the water oxidizing complex of Photosystem II at liquid helium temperatures produces the metalloradical intermediate attributed to S1YZ. Biochemistry 42 (2003) 3045-3053
37. Boussac A., Un S., Horner O., and Rutherford A.W. High-spin states (S > = 5/2) of the photosystem II manganese complex. Biochemistry 37 (1998) 4001-4007
38. 0* state in photosystem II. Biochemistry 36 (1997) 11055-11060
39. Hillier W., and Wydrzynski T. Substrate water interactions within the photosystem II oxygen evolving complex. Phys. Chem. Chem. Phys. 6 (2004) 4882-4889
40. Messinger J., Badger M., and Wydrzynski T. Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 3209-3213
41. Sproviero E.M., Gascon J.A., McEvoy J.P., Brudvig G.W., and Batista V.S. Characterization of synthetic oxomanganese complexes and the inorganic core of the O2-evolving complex in photosystem II: evaluation of the DFT/B3LYP level of theory. J. Inorg. Biochem. 100 (2006) 786-800
42. Siegbahn P.E.M. Mechanisms of metalloenzymes studied by quantumchemical methods. Quart. Rev. Biophys. 36 (2003) 91-145
43. Ishikita H., Saenger W., Biesiadka J., Loll B., and Knapp E.W. How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9855-9860
44. Grabolle M., and Dau H. Energetics of primary and secondary electron transfer in Photosystem II membrane particles of spinach revisited on basis of recombination-fluorescence measurements. Biochim. Biophys. Acta 1708 (2005) 209-218
45. Pospisil P., and Dau H. Chlorophyll fluorescence transients of Photosystem II membrane particles as a tool for studying photosynthetic oxygen evolution. Photosynth. Res. 65 (2000) 41-52
46. Rutherford A.W., Govindjee, and Inoue Y. Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proc. Natl. Acad. Sci. U. S. A. 81 (1983) 1107-1111
47. Hou J.M., Boichenko V.A., Diner B.A., and Mauzerall D. Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: volume change, enthalpy, and entropy of electron-transfer reactions in manganese-depleted photosystem II core complexes. Biochemistry 40 (2001) 7117-7125
48. Dau H., and Hansen U.P. A study on the energy-dependent quenching of chlorophyll fluorescence by means of photoacoustic measurements. Photosynth. Res. 25 (1990) 269-278
49. Zankel K. Rapid delayed luminescence from chloroplasts: kinetic analysis of components; the relationship to the O 2 evolving system. Biochim. Biophys. Acta 245 (1971) 373-385
50. Govindjee, Pulles M.P., Govindjee R., Van Gorkom H.J., and Duysens L.N. Inhibition of the reoxidation of the secondary electron acceptor of photosystem II by bicarbonate depletion. Biochim. Biophys. Acta 449 (1976) 602-605
51. Shinkarev V.P., and Govindjee. Insight into the relationship of chlorophyll a fluorescence yield to the concentration of its natural quenchers in oxygenic photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 7466-7469
52. Murray J.W., and Barber J. Identification of a calcium-binding site in the PsbO protein of photosystem II. Biochemistry 45 (2006) 4128-4130
53. Ishikita H., Saenger W., Loll B., Biesiadka J., and Knapp E.W. Energetics of a possible proton exit pathway for water oxidation in photosystem II. Biochemistry 45 (2006) 2063-2071
54. Hays A.M., Vassiliev I.R., Golbeck J.H., and Debus R.J. Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37 (1998) 11352-11365
55. Kok B., Forbush B., and McGloin M. Cooperation of charges in photosynthetic O2 evolution-I. A linear four-step mechanism. Photochem. Photobiol. 11 (1970) 457-475
56. Hoganson C.W., and Babcock G.T. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277 (1997) 1953-1956
57. Dau H., and Haumann M. Reaction cycle of photosynthetic water oxidation in plant and cyanobacteria. Science 312 (2006) 1471-1472
58. Penner-Hahn J.E., and Yocum C.F. The photosynthesis "oxygen clock" gets a new number. Science 310 (2005) 982-983
59. H. Dau, M. Haumann, Time-resolved X-ray spectroscopy leads to an extension of the classical S-state cycle model of photosynthetic oxygen evolution, Photosynth. Res. in press (Published online http://www.springerlink.com/content/g32t04851m61655g/).
60. Dau H., and Haumann M. Reaction cycle of photosynthetic water oxidation in plants and cyanobacteria. Science 312 (2006) 1471-1472
61. Babcock G.T., Blankenship R.E., and Sauer K. Reaction kinetics for positive charge accumulation on the water side of chloroplast photosystem II. FEBS Lett. 61 (1976) 286-289
62. Razeghifard M.R., and Pace R.J. Electron paramagnetic resonance kinetic studies of the S states in spinach PSII membranes. Biochim. Biophys. Acta 1322 (1997) 141-150
63. Witt H.T., Schlodder E., Brettel K., and Saygin T.M. Reaction sequences from light absorption to the cleavage of water in photosynthesis, routes, rates and intermediates. Photosynth. Res. 10 (1986) 453-471
64. Junge W. In: Goodwin T.W. (Ed). Chemistry and Biochemistry of Plant Pigments (1976), Academic Press, London 233-333
65. Junge W., Haumann M., Ahlbrink R., Mulkidjanian A., and Clausen J. Electrostatics and proton transfer in photosynthetic water oxidation. Philos. Trans. R. Soc. London, Ser. B 357 (2002) 1407-1418
66. Lavergne J. Optical-difference spectra of the S-state transitions in the photosynthetic oxygen-evolving complex. Biochim. Biophys. Acta 894 (1987) 91-107
67. Dekker J.P., Plijter J.J., Ouwehand L., and van Gorkom H.J. Kinetics of manganese redox transitions in the oxygen evolving apparatus of photosynthesis. Biochim. Biophys. Acta 767 (1984) 176-179
68. Renger G., and Weiss W. The detection of intrinsic 320(nm absorption changes reflecting the turnover of the water-splitting enzyme system Y which leads to oxygen formation in trypsinized chloroplasts. FEBS Lett. 137 2 (1982) 217-221
69. Haumann M., Müller C., Liebisch P., Neisius T., and Dau H. A novel BioXAS technique with sub-millisecond time resolution to track oxidation state and structural changes at biological metal centers. J. Synchrotron Radiat. 12 (2005) 35-44
70. Schlodder E., and Witt H.T. Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation. Reexamination By a glass electrode study at pH 5.5-7.2. J. Biol. Chem. 274 (1999) 30387-30392
71. Lavergne J., and Junge W. Proton release during the redox cycle of the water oxidase. Photosynth. Res. 38 (1993) 279-296
72. Haumann M., and Junge W. In: Ort D., and Yocum C.F. (Eds). Oxygenic Photosynthesis-The Light Reactions (1996), Kluwer Academic Publ., Dordrecht 165-192
73. Haumann M., Boegershausen O., and Junge W. Photosynthetic oxygen evolution: net charge transients as inferred from electrochromic bandshifts are independent of proton release into the medium. FEBS Lett. 355 (1994) 101-105
74. Witt H.T., and Zickler A. Vectorial electron flow across the thylakoid membrane. Further evidence by kinetic measurements with an electrochromic and electrical method. FEBS Lett. 39 (1974) 205-208
75. Saygin O., and Witt H.T. Evidence for the electrochromic identification of the change of charges in the four oxidation steps of the photoinduced water cleavage in photosynthesis. FEBS Lett. 187 2 (1985) 224-ff
76. Emrich H.M., Junge W., and Witt H.T. Further evidence for an optical response of chloroplast bulk pigments to a light-induced electrical field in photosynthesis. Z. Naturforsch. 24 (1969) 1144-1146
77. Dismukes G.C., and Siderer Y. Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc. Natl. Acad. Sci. U. S. A. 78 (1981) 274-278
78. Goodin D.B., Yachandra V.K., Britt R.D., Sauer K., and Klein M.P. The state of manganese in the photosynthetic apparatus. 3. Light-induced changes in X-ray absorption (K-edge) energies of manganese in photosynthetic membranes. Biochim. Biophys. Acta 767 (1984) 209-216
79. Fowler C.F. Proton evolution from photosystem II. Stoichiometry and mechanistic considerations. Biochim. Biophys. Acta 462 (1977) 414-421
80. Saphon S., and Crofts A.R. Protolytic reactions in photosystem II: a new model for the release of protons accompanying the photooxidation of water. Z. Naturforsch. 32C (1977) 617-626
81. Wille B., and Lavergne J. Measurement of proton translocation in the thylakoids under flashing light using a spin-labelled amine. Photobiochem. Photobiophys. 4 (1982) 131-144
82. Bowes J.M., and Crofts A.R. Interactions of protons with transitions of the watersplitting enzyme of photosystem II as measured by delayed fluorescence. Z. Naturforsch. 33c (1978) 271-275
83. Förster V., and Junge W. Stoichiometry and kinetics of proton release upon photosynthetic water oxidation. Photochem. Photobiol. 41 (1985) 183-190
84. Kretschmann H., and Witt H.T. Chemical reduction of the water splitting enzyme system of photosynthesis and its light-induced reoxidation characterized by optical and mass spectroscopical measurements: a basis for the estimation of the states of redox active manganese and of water in the quarternary oxygen-evolving S-state cycle. Biochim. Biophys. Acta 1144 (1993) 331-345
85. Kretschmann H., Schlodder E., and Witt H.T. Net charge oscillation and proton release during water oxidation in photosynthesis. An electrochromic band shift study at pH 5.5-7.0. Biochim. Biophys. Acta 1274 (1996) 1-8
86. Haumann M., Bögershausen O., Cherepanov D., Ahlbrink R., and Junge W. 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 (1997) 93-208
87. Renger G., and Hanssum B. Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett. 299 (1992) 28-32
88. Miller A.F., and Brudvig G.W. A guide to electron paramagnetic resonance spectroscopy of photosystem II membranes. Biochim. Biophys. Acta 1056 (1991) 1-18
89. De Paula J.C., Innes J.B., and Brudvig G.W. Electron transfer in photosystem II at cryogenic temperatures. Biochemistry 24 (1985) 8114-8120
90. Witt H.T. Primary reactions of oxygenic photosynthesis. Ber. Bunsenges. Phys. Chem. 100 (1996) 1923-1942
91. Rappaport F., Blanchard-Desce M., and Lavergne J. Kinetics of electron transfer and electrochromic change during the redox transition of the photosynthetic oxygen-evolving complex. Biochim. Biophys. Acta 1184 (1994) 178-192
92. Razeghifard M.R., and Pace R.J. EPR kinetic studies of oxygen release in thylakoids and PSII membranes: an intermediate in the S3 to S0 transition. Biochemistry 38 (1999) 1252-1257
93. M. Grabolle, Die Donorseite des Photosystems II: Rekombinationsfluoreszenz- und Röntgenabsorptionsstudien (thesis), FB Physik, Free Univ. Berlin (2005).
94. 0) characterized by X-ray absorption spectroscopy at 20 K as well as at room temperature. Biochemistry 44 (2005) 1894-1908
95. Haumann M., and Junge W. Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. Biochemistry 33 (1994) 864-872
96. Bernat G., Morvaridi F., Feyziyev Y., and Styring S. pH-dependence of the four individual transitions in the catalytic S-cycle during photosynthetic oxygen evolution. Biochemistry 41 (2002) 5830-5843
97. Messinger J., Schroder W.P., and Renger G. Structure-function relations in photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry 32 (1993) 7658-7668
98. Vass I., and Styring S. pH-Dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30 (1991) 830-839
99. Junge W., and Clausen J. Photosynthetic oxygen production (Letter). Science 312 (2006) 1470-1471
100. Clausen J., and Junge W. Detection of an intermediate of photosynthetic water oxidation. Nature 430 (2004) 480-483
101. Clausen J., Junge W., Dau H., and Haumann M. Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44 (2005) 12775-12779
102. Penner-Hahn J.E., and Yocum C.F. Photosynthetic oxygen production (Response). Science 312 (2006) 1470-1471
103. Messinger J., Seaton G., Wydrzynski T., Wacker U., and Renger G. S-3 state of the water oxidase in photosystem II. Biochemistry 36 (1997) 6862-6873
104. Barra M., Haumann M., Loja P., Krivanek R., Grundmeier A., and Dau H. Intermediates in assembly by photoactivation after thermally accelerated disassembly of the manganese complex of photosynthetic water oxidation. Biochemistry 45 (2006) 14523-14532
105. Ahlbrink R., Haumann M., Cherepanov D., Boegershausen O., Mulkidjanian A., and Junge W. Function of tyrosine-Z in water oxidation by photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry 37 (1998) 1131-1142
106. Dau H., and Haumann M. Considerations on the mechanism of photosynthetic water oxidation - dual role of oxo-bridges between Mn ions in (i) redox-potential maintenance and (ii) proton abstraction from substrate water. Photosynth. Res. 84 (2005) 325-331
107. Rappaport F., Guergova-Kuras M., Nixon P.J., Diner B.A., and Lavergne J. Kinetics and pathways of charge recombination in Photosystem II. Biochemistry 41 (2002) 8518-8527
108. Magnuson A., Liebisch P., Hogblom J., Anderlund M.F., Lomoth R., Meyer-Klaucke W., Haumann M., and Dau H. Bridging-type changes facilitate successive oxidation steps at about 1 V in two binuclear manganese complexes-implications for photosynthetic water-oxidation. J. Inorg. Biochem. 100 (2006) 1234-1243
109. Krishtalik L.I. Energetics of multielectron reactions. Photosynthetic oxygen evolution. Biochim. Biophys. Acta 849 (1986) 162-171
110. Krishtalik L.I. Energetics of the reaction of photosynthetic evolution of oxygen. Biofizika 34 (1989) 883-886
111. Hendry G., and Wydrzynski T. The two substrate-water molecules are already bound to the oxygen-evolving complex in the S2-state of Photosystem II. Biochemistry 41 (2002) 13328-13334
112. Hillier W., Messinger J., and Wydrzynski T. Kinetic determination of the fast exchanging substrate water molecule in the S3 state of photosystem II. Biochemistry 37 (1998) 16908-16914
113. McEvoy J.P., and Brudvig G.W. Structure-based mechanism of photosynthetic water oxidation. Phys. Chem. Chem. Phys. 6 (2004) 4754-4763
114. Siegbahn P.E.M., and Crabtree R.H. 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 (1999) 117-127