The mechanism of photosynthetic water splitting

Photochemical and Photobiological Sciences

Volumn 4, Issue 12, 2005, Pages 940-949

  McEvoy, James P ^a   Gascon, Jose A ^a   Batista, Victor S ^a   Brudvig, Gary W ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; MANGANESE; WATER;

ATMOSPHERE; BIOSPHERE; CATALYSIS; ENERGY TRANSFER; MEMBRANE TRANSPORT; OXIDATION; OXYGENATION; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; X RAY CRYSTALLOGRAPHY;

CYANOBACTERIA; VIRIDIPLANTAE;

EID: 29244484289     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/b506755c     Document Type: Article

References (98)

1. P. Joliot and B. Kok, Oxygen evolution in photosynthesis, in Bioenergetics of Photosynthesis, ed. Govindjee, Academic Press, New York, 1975, pp. 387–412.
2. C. F. Yocum C. T. Yerkes R. E. Blankenship R. R. Sharp G. T. Babcock Stoichiometry, inhibitor sensitivity, and organization of manganese associated with photosynthetic oxygen evolution Proc. Natl. Acad. Sci. U. S. A. 1981 78 7507-7511.
3. 2 evolution and system II Biochim. Biophys. Acta 1970 197 219-239.
4. G. W. Brudvig Electron paramagnetic resonance spectroscopy Methods Enzymol. 1995 246 536-554.
5. R. D. Britt J. M. Peloquin K. A. Campbell Pulsed and parallel-polarization EPR characterization of the photosystem II oxygen-evolving complex Annu. Rev. Biophys. Biomol. Struct. 2000 29 463-495.
6. A. Boussac S. Un O. Horner A. W. Rutherford High-spin states (S > = 5/2) of the photosystem II manganese complex Biochemistry 1998 37 4001-4007.
7. H. Dau P. Liebisch M. Haumann 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. 2003 376 562-583.
8. V. K. Yachandra Structure of the manganese complex in photosystem II: insights from X-ray spectroscopy Philos. Trans. R. Soc. London, Ser. B 2002 357 1347-1357.
9. J. E. Penner-Hahn Structural characterization of the Mn site in the photosynthetic oxygen-evolving complex Struct. Bonding 1998 90 1-36.
10. B. Ke, Photosynthesis: Photobiochemistry and Photobiophysics, ed. Govindjee, Kluwer Academic Publishers, Dordrecht, 2001.
11. J. Clausen W. Junge Detection of an intermediate of photosynthetic water oxidation Nature 2004 430 480-483.
12. C. Berthomieu R. Hienerwadel A. Boussac J. Breton B. A. Diner Hydrogen bonding of redox-active tyrosine Z of photosystem II probed by FTIR difference spectroscopy Biochemistry 1998 37 10547-10554.
13. 2 transition: an isotope-edited FTIR study Biochemistry 2004 43 3152-3166.
14. T. Noguchi M. Sugiura Structure of an active water molecule in the water-oxidizing complex of photosystem II as studied by FTIR spectroscopy Biochemistry 2000 39 10943-10949.
15. J. Clausen R. J. Debus W. Junge Time-resolved oxygen production by PSII: chasing chemical intermediates Biochim. Biophys. Acta 2004 1655 184-194.
16. M. Haumann and W. Junge, Proton and charge indicators in oxygen evolution, in Oxygenic Photosynthesis: The Light Reactions, ed. D. R. Ort and C. F. Yocum, Kluwer Academic Publishers, Dordrecht, 1996, pp. 165–192.
17. W. Hillier T. Wydrzynski Substrate water interactions within the photosystem II oxygen evolving complex Phys. Chem. Chem. Phys. 2004 6 4882-4889.
18. 2 evolving complex of photosystem II vary independently during S-state turnover Biochemistry 2000 39 4399-4405.
19. A. Zouni H. T. Witt J. Kern P. Fromme N. Krauss W. Saenger P. Orth Crystal structure of photosystem II from Synechococcus elongatus at 3.8 ångström resolution Nature 2001 409 739-743.
20. N. Kamiya J. R. Shen Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 ångström resolution Proc. Natl. Acad. Sci. U. S. A. 2003 100 98-103.
21. J. Biesiadka B. Loll J. Kern K. D. Irrgang A. Zouni Crystal structure of cyanobacterial photosystem II at 3.2 ångström resolution: a closer look at the Mn-cluster Phys. Chem. Chem. Phys. 2004 6 4733-4736.
22. K. N. Ferreira T. M. Iverson K. Maghlaoui J. Barber S. Iwata Architecture of the photosynthetic oxygen-evolving center Science 2004 303 1831-1838.
23. M. Pourbaix, Atlas of Electrochemical Equilibria, Pergamon Press, Oxford, 1966.
24. D. M. Kramer C. A. Sacksteder J. A. Cruz How acidic is the lumen? Photosynth. Res. 1999 60 151-163.
25. L. I. Krishtalik Energetics of multielectron reactions-photosynthetic oxygen evolution Biochim. Biophys. Acta 1986 849 162-171.
26. G. Renger Model for molecular mechanism of photosynthetic oxygen evolution FEBS Lett. 1977 81 223-228.
27. Z in photosynthetic oxygen evolution Photosynth. Res. 1995 46 177-184.
28. J. G. Metz P. J. Nixon M. Rogner G. W. Brudvig B. A. Diner 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 1989 28 6960-6969.
29. + in photosystem II is tyrosine-161 of the D1 polypeptide Biochemistry 1988 27 9071-9074.
30. M. Haumann W. Junge Extent and rate of proton release by photosynthetic water oxidation in thylakoids-electrostatic relaxation versus chemical production Biochemistry 1994 33 864-872.
31. F. Mamedov R. T. Sayre S. Styring Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of photosystem II Biochemistry 1998 37 14245-14256.
32. A. M. A. Hays I. R. Vassiliev J. H. Golbeck R. J. Debus Role of D1–His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study Biochemistry 1998 37 11352-11365.
33. C. W. Hoganson G. T. Babcock A metalloradical mechanism for the generation of oxygen from water in photosynthesis Science 1997 277 1953-1956.
34. 2 formation Biochemistry 2001 40 7937-7945.
35. 2+ J. Chin. Chem. Soc. (Taipei) 2004 51 1221-1228.
36. 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 2003 42 6209-6217.
37. 4Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of photosystem II membranes Biochemistry 2004 43 13271-13282.
38. 87Sr ESEEM spectroscopy J. Am. Chem. Soc. 2004 126 7228-7237.
39. J. P. McEvoy G. W. Brudvig Structure-based mechanism of photosynthetic water oxidation Phys. Chem. Chem. Phys. 2004 6 4754-4763.
40. J. S. Vrettos J. Limburg G. W. Brudvig Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry Biochim. Biophys. Acta 2001 1503 229-245.
41. J. P. McEvoy, J. A. Gascon, E. M. Sproviero, V. S. Batista and G. W. Brudvig, Computational structural model of the oxygen evolving complex in photosystem II: Complete ligation by protein, water and chloride, in Photosynthesis: Fundamental Aspects to Global Perspectives, ed. D. Bruce and A. van der Est, Allen Press, Lawrence, Kansas, 2005, vol. 1, pp. 278–280.
42. 1 state-EXAFS results in relation to recent crystallographic data Phys. Chem. Chem. Phys. 2004 6 4781-4792.
43. F. A. Cotton and G. Wilkinson, Advanced Inorganic Chemistry, Wiley-Interscience, New York, 1999.
44. A. K. Katz J. P. Glusker S. A. Beebe C. W. Bock Calcium ion coordination: A comparison with that of beryllium, magnesium, and zinc J. Am. Chem. Soc. 1996 118 5752-5763.
45. K. Lindberg L. E. Andreasson A one-site, two-state model for the binding of anions in photosystem II Biochemistry 1996 35 14259-14267.
46. Z in water-splitting Biochemistry 1997 36 12062-12070.
47. K. Olesen L. E. Andreasson The function of the chloride ion in photosynthetic oxygen evolution Biochemistry 2003 42 2025-2035.
48. J. Dasgupta R. T. van Willigen G. C. Dismukes Consequences of structural and biophysical studies for the molecular mechanism of photosynthetic oxygen evolution: functional roles for calcium and bicarbonate Phys. Chem. Chem. Phys. 2004 6 4793-4802.
49. P. J. Nixon J. T. Trost B. A. Diner Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis Sp Pcc 6803-assembly requires a free carboxyl group at C-terminal position 344 Biochemistry 1992 31 10859-10871.
50. 2+ depletion and metal cation substitution in the photosynthetic oxygen-evolving complex Biochemistry 2002 41 5844-5853.
51. M. A. Strickler L. M. Walker W. Hillier R. J. Debus Evidence from biosynthetically incorporated strontium and FTIR difference spectroscopy that the C-terminus of the D1 polypeptide of photosystem II does not ligate calcium Biochemistry 2005 44 8571-8577.
52. Y. Kimura N. Mizusawa T. Yamanari A. Ishii T. Ono Structural changes of D1 C-terminal alpha-carboxylate during S-state cycling in photosynthetic oxygen evolution J. Biol. Chem. 2005 280 2078-2083.
53. R. D. Britt K. A. Campbell J. M. Peloquin M. L. Gilchrist C. P. Aznar M. M. Dicus J. Robblee J. Messinger Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms Biochim. Biophys. Acta 2004 1655 158-171.
54. Z in manganese-depleted photosystem II Biochemistry 1999 38 11851-11865.
55. R. A. Roffey D. M. Kramer Govindjee R. T. Sayre Lumenal side histidine mutations in the D1 protein of photosystem II affect donor side electron-transfer in Chlamydomonas reinhardtii Biochim. Biophys. Acta 1994 1185 257-270.
56. Z of PSII, in Photosynthesis: Mechanisms and Effects, ed. G. Garab, Kluwer Academic Publishers, Dordrecht, 1998, vol. 2, pp. 1177–1180.
57. X. S. Tang D. A. Chisholm G. C. Dismukes G. W. Brudvig B. A. Diner Spectroscopic evidence from site-directed mutants of Synechocystis PCC6803 in favor of a close interaction between histidine 189 and redox-active tyrosine 160, both of polypeptide D2 of the photosystem II reaction center Biochemistry 1993 32 13742-13748.
58. C. Tommos G. T. Babcock Proton and hydrogen currents in photosynthetic water oxidation Biochim. Biophys. Acta 2000 1458 199-219.
59. F. Rappaport J. Lavergne Charge recombination and proton transfer in manganese-depleted photosystem II Biochemistry 1997 36 15294-15302.
60. F. Rappaport M. Blanchard-Desce J. Lavergne Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex Biochim. Biophys. Acta 1994 1184 178-192.
61. J. Lavergne W. Junge Proton release during the redox cycle of the water oxidase Photosynth. Res. 1993 38 279-296.
62. V. Petrouleas D. Koulougliotis N. Ioannidis Trapping of metalloradical intermediates of the S-states at liquid helium temperatures. Overview of the phenomenology and mechanistic implications Biochemistry 2005 44 6723-6728.
63. C. G. Mowat R. Moysey C. S. Miles D. Leys M. K. Doherty P. Taylor M. D. Walkinshaw G. A. Reid S. K. Chapman Kinetic and crystallographic analysis of the key active site acid/base arginine in a soluble fumarate reductase Biochemistry 2001 40 12292-12298.
64. M. K. Doherty S. L. Pealing C. S. Miles R. Moysey P. Taylor M. D. Walkinshaw G. A. Reid S. K. Chapman Identification of the active site acid/base catalyst in a bacterial fumarate reductase: A kinetic and crystallographic study Biochemistry 2000 39 10695-10701.
65. 2 transitions Biochemistry 1997 36 3663-3670.
66. 0) characterized by X-ray absorption spectroscopy at 20 K and room temperature Biochemistry 2005 44 1894-1908.
67. 2OH are consistent with a Mn(III)/Mn(III)/Mn(IV)/Mn(IV) oxidation state for the dark-adapted enzyme Biochemistry 2005 44 2129-2142.
68. H. Dau L. Iuzzolino J. Dittmer The tetra-manganese complex of photosystem II during its redox cycle-X-ray absorption results and mechanistic implications Biochim. Biophys. Acta 2001 1503 24-39.
69. V. K. Yachandra V. J. DeRose M. J. Latimer I. Mukerji K. Sauer M. P. Klein Where plants make oxygen - a structural model for the photosynthetic oxygen-evolving manganese cluster Science 1993 260 675-679.
70. 3 transitions of the water oxidation cycle Biochemistry 1998 37 17112-17119.
71. T. A. Roelofs W. C. Liang M. J. Latimer R. M. Cinco A. Rompel J. C. Andrews K. Sauer V. K. Yachandra M. P. Klein Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex Proc. Natl. Acad. Sci. U. S. A. 1996 93 3335-3340.
72. 2 state of the photosynthetic oxygen-evolving complex - an X-ray absorption-edge spectroscopy study Biochim. Biophys. Acta 1987 890 395-398.
73. T. G. Carrell A. M. Tyryshkin G. C. Dismukes An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures J. Biol. Inorg. Chem. 2002 7 2-22.
74. D. Kuzek R. J. Pace Probing the Mn oxidation states in the OEC. Insights from spectroscopic, computational and kinetic data Biochim. Biophys. Acta 2001 1503 123-137.
75. 3 transition: implications for the mechanism of photosynthetic water oxidation J. Am. Chem. Soc. 2001 123 7804-7820.
76. 0 state of the oxygen evolving complex in photosystem II Biochemistry 1997 36 13148-13152.
77. 0 state of the oxygen-evolving complex in photosystem II is paramagnetic: detection of EPR multiline signal J. Am. Chem. Soc. 1997 119 11349-11350.
78. 0 state in photosystem II Biochemistry 1997 36 11055-11060.
79. 1 states determined by X-ray absorption spectroscopy Biochemistry 1990 29 486-496.
80. 2 states of the oxygen-evolving complex in photosystem II J. Am. Chem. Soc. 2005 127 2392-2393.
81. V. L. Pecoraro M. J. Baldwin M. T. Caudle W. Y. Hsieh N. A. Law A proposal for water oxidation in photosystem II Pure Appl. Chem. 1998 70 925-929.
82. J. M. Workman R. D. Powell A. D. Procyk T. J. Collins D. F. Bocian Vibrational and electrochemical properties of a series of stable manganese(V)-oxo complexes Inorg. Chem. 1992 31 1548-1550.
83. T. J. Collins R. D. Powell C. Slebodnick E. S. Uffelman A water-stable manganese(V)-oxo complex-definitive assignment of a v(Mn(V)O) infrared vibration J. Am. Chem. Soc. 1990 112 899-901.
84. T. J. Collins S. W. Gordon-Wylie A manganese(V)-oxo complex J. Am. Chem. Soc. 1989 111 4511-4513.
85. C. G. Miller S. W. Gordon-Wylie C. P. Horwitz S. A. Strazisar D. K. Peraino G. R. Clark S. T. Weintraub T. J. Collins A method for driving O-atom transfer: secondary ion binding to a tetraamide macrocyclic ligand J. Am. Chem. Soc. 1998 120 11540-11541.
86. F. M. MacDonnell N. L. P. Fackler C. Stern T. V. O’Halloran Air oxidation of a 5-coordinate Mn(III) dimer to a high-valent oxomanganese(V) complex J. Am. Chem. Soc. 1994 116 7431-7432.
87. 2 complexes Photosynth. Res. 1993 38 303-308.
88. 3 transitions in photosystem II Biochemistry 2005 44 1367-1374.
89. T. Kambara Govindjee Molecular mechanism of water oxidation in photosynthesis based on the functioning of manganese in two different environments Proc. Natl. Acad. Sci. U. S. A. 1985 82 6119-6123.
90. G. W. Brudvig H. H. Thorp R. H. Crabtree Probing the mechanism of water oxidation in photosystem II Acc. Chem. Res. 1991 24 311-316.
91. 2 state of photosystem II Biochemistry 2002 41 13328-13334.
92. d for water exchange on divalent octahedral metal ions going from manganese(II) to nickel(II) Inorg. Chem. 1980 19 3696-3703.
93. F. C. Xu H. R. Krouse T. W. Swaddle Conjugate base pathway for water exchange on aqueous chromium(III)-variable-pressure and variable-temperature kinetic study Inorg. Chem. 1985 24 267-270.
94. D. T. Richens, The Chemistry of Aqua Ions, John Wiley and Sons, Chichester, 1997.
95. 3 state of photosystem II Biochemistry 1998 37 16908-16914.
96. 17O NMR study Magn. Reson. Chem. 1997 35 765-773.
97. G. Atkinson M. M. Emara R. Fernande Ultrasonic absorption in aqueous solutions of calcium acetate and other bivalent metal acetates J. Phys. Chem. 1974 78 1913-1917.
98. R. Tagore, H. Chen, R. H. Crabtree and G. W. Brudvig, 2005, manuscript submitted.