Coupling of electron and proton transfer in oxidative water cleavage in photosynthesis

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1655, Issue 1-3, 2004, Pages 195-204

  Renger, G ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

O O bond formation; Primary donor; Redox active tyrosine; Redox isomerism; Tautomerism; Water cleavage

Indexed keywords

MATRIX PROTEIN; WATER;

CATALYSIS; CATALYST; CHEMICAL BOND; ELECTRON TRANSPORT; ELECTRONICS; MOLECULAR DYNAMICS; OXIDATION; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW;

ELECTRON TRANSPORT; KINETICS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTON-MOTIVE FORCE; TYROSINE; WATER;

MUS;

EID: 1942472529     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2003.07.007     Document Type: Review

References (115)

1. G. Renger, Molecular mechanism of water oxidation, in: G.S. Singhal, G. Renger, Govindjee, K.-D. Irrgang, S.K. Sopory (Eds.), Concepts in Photobiology: Photosynthesis and Photomorphogenesis, Kluwer Academic Publishing, Dordrecht, Narosa Publishing, Delhi, 1999, pp. 292-329.
2. Zouni A., Witt H.T., Kern J., Fromme P., Krauß N., Saenger W., Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature. 409:2001;739-743.
3. Kamiya N., 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.
4. 2 evolution. Biochim. Biophys. Acta. 1102:1992;269-352.
5. Yachandra V.K., Sauer K., Klein M.P. Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem. Rev. 96:1996;2927-2950.
6. Bricker T.M., Frankel L.K. The structure and function of CP47 and CP43 in photosystem II. Photosynth. Res. 72:2002;131-146.
7. Enami I., Kikuchi S., Fukuda S., Ohta H., Shen J.R. Binding and functional properties of four extrinsic proteins of photosystem II from a red alga, Cyanidium caldarium, as studied by release-reconstitution experiments. Biochemistry. 37:1998;2787-2793.
8. 2 evolution: I. A linear four-step mechanism. Photochem. Photobiol. 11:1970;457-475.
9. -3 state of the water oxidase in photosystem II. Biochemistry. 36:1997;6862-6873.
10. Messinger J., Robblee J.H., Bergmann U., Fernandez C., Glatzel P., Isgandarova S., Hanssum B., Renger G., Cramer S.P., Sauer K., Yachandra V.K. Manganese oxidation states in photosystem II. Proc. 12th Int. Congr. Photosynthesis. 2001;CSIRO Publishing, Collingwood, Australia. S10-019.
11. Renger G. Mechanistic and structural aspects of photosynthetic water oxidation. Physiol. Plant. 100:1997;828-841.
12. 4-cluster of photosynthetic oxygen evolving complex. Biochim. Biophys. Acta. 1503:2001;40-51.
13. Renger G. Water cleavage by solar radiation - an inspiring challenge of photosynthesis research. Photosynth. Res. 38:1993;229-247.
14. Renger G. Apparatus and mechanism of photosynthetic oxygen evolution: a personal perspective. Photosynth. Res. 76:2003;269-288.
15. Barry B., Babcock G.T. Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. U. S. A. 84:1987;7099-7103.
16. + in Photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry. 27:1988;9071-9074.
17. Babcock G.T., Barry B.A., Debus R.J., Hoganson C.W., Atamian M., McIntosh L., Sithole U., Yocum C.G. Water oxidation in Photosystem II: from radical chemistry to multielectron chemistry. Biochemistry. 28:1989;9557-9565.
18. + decay kinetics in tris-washed chloroplast photosystem II preparations as a function of pH. Biochim. Biophys. Acta. 722:1983;327-330.
19. Weiss W., Renger G. On the functional connection between the reaction center complex and the water oxidizing enzyme system Y. Biochim. Biophys. Acta. 850:1986;173-183.
20. II and the water-oxidizing manganese complex. FEBS Lett. 237:1988;69-75.
21. Renger G., Wolff Ch. The existence of a high photochemical turnover rate at the reaction centers of system II in Tris-washed chloroplasts. Biochim. Biophys. Acta. 423:1976;610-614.
22. Haveman J., Mathis P. Flash-induced absorption changes of the primary donor of photosystem II at 820 nm in chloroplasts inhibited by low pH or tris-treatment. Biochim. Biophys. Acta. 440:1976;346-355.
23. Conjeaud H., Mathis P., Paillotin G. The effect of pH on the reduction kinetics of P-680 in tris-treated chloroplasts. Biochim. Biophys. Acta. 48:1979;280-291.
24. Renger G. A rapid vectorial back reaction at the reaction centers of photosystem II in tris-washed chloroplasts induced by repetitive flash excitation. Biochim. Biophys. Acta. 547:1979;103-116.
25. Christen G., Karge M., Eckert H.-J., Renger G. The role of protonation steps in electron transfer reactions in Tris-treated PS II membrane fragments. Photosynthetica. 33:1997;529-539.
26. +· reduction kinetics and redox transition probability of the water oxidising complex as a function of pH and H/D isotope exchange in spinach thylakoids. Biochemistry. 38:1999;6082-6092.
27. Messinger J., Schröder W.P., 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.
28. Isgandarova S., Renger G., Messinger J. Functional differences of photosystem II from Synechococcus elongatus and spinach characterized by flash-induced oxygen evolution patterns. Biochemistry. 42:2003;8929-8938.
29. Gläser M., Wolff Ch., Renger G. Indirect evidence for a very fast recovery kinetics of chlorophyll-a II in spinach chloroplasts. Z. Naturforsch. 31c:1976;712-721.
30. Renger G., Eckert H.J., Weiss W. Studies on the mechanism of photosynthetic oxygen formation. Inoue Y., Crofts A.R., Govindjee, Murata N., Renger G., Satoh K. The Oxygen Evolving System in Photosynthesis. 1983;73-82 Academic Press, Japan.
31. 2-evolving complex. Biochim. Biophys. Acta. 766:1984;403-415.
32. i of the water oxidizing system. FEBS Lett. 236:1988;425-431.
33. Ahlbrink R., Haumann M., Cherepanov D., Bögershausen D., Mulkidjanian O., Junge W. Function of tyrozine Z in water oxidation by Photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry. 37:1998;1131-1142.
34. Reinman S., Mathis P. Influence of temperature on photosystem II electron transfer reactions. Biochim. Biophys. Acta. 635:1981;249-258.
35. Renger G., Christen G., Karge M., Eckert H.-J., Irrgang K.-D. Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation - results and implications. JBIC. 3:1998;360-366.
36. Lavergne J., Rappaport F. Stabilization of charge separation and photochemical misses in photosystem II. Biochemistry. 37:1998;7899-7906.
37. Vermaas W.C.J., Renger G., Dohnt G. The reduction of the oxygen-evolving system in chloroplasts by thylakoid components. Biochim. Biophys. Acta. 764:1984;194-202.
38. van Best J.A., Mathis P. Kinetics of reduction of the oxidized primary electron donor of photosystem II in spinach chloroplasts and in chlorella cells in the microsecond and nanosecond time ranges following flash excitation. Biochim. Biophys. Acta. 503:1978;178-188.
39. Renger G., Eckert H.J., Hagemann R., Hanssum B., Koike H., Wacker U. New results on the mechanism of photosynthetic water oxidation. Singhal G.S., Barber J., Dilley R.A., Govindjee, Haselkorn R., Mohanty P. Photosynthesis: Molecular Biology and Bioenergetics. 1989;357-371 Narosa Publ. House, New Delhi.
40. + reduction kinetics during water splitting. Garab G. Photosynthesis and Effects. vol. II:1998;1045-1048 Kluwer Academic Publishing, Dordrecht.
41. + reduction in oxygen-evolving Photosystem II. Biochemistry. 41:2002;5015-5023.
42. Chu H.-A., Nguyen A.P., Debus R.J. Amino acid residues that influence the binding of manganese or calcium to Photosystem II: 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry. 34:1995;5839-5858.
43. Mamedov F., Sayre R.T., Styring S. Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of Photosystem II. Biochemistry. 37:1998;14245-14256.
44. Berthomieu C., Hienerwadel R., Boussac A., Breton J., Diner B.A. Hydrogen bonding of redox-active tyrosine Z of Photosystem II probed by FTIR difference spectroscopy. Biochemistry. 37:1998;10547-10554.
45. Hays A.-M.A., Vassiliev I.R., Golbeck J.H., 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.
46. Z in manganese-depleted Photosystem II. Biochemistry. 38:1999;11851-11865.
47. Marcus R.A., Sutin N. Electron transfer in chemistry and biology. Biochim. Biophys. Acta. 811:1985;265-322.
48. Tommos C., Babcock G.T. Oxygen production in nature: a light-driven metalloradical enzyme process. Acc. Chem. Res. 31:1998;18-25.
49. Karge M., Irrgang K.-D., Sellin S., Feinäugle R., Liu B., Eckert H.-J., Eichler H.J., Renger G. Effects of hydrogen/deuterium exchange on photosynthetic water cleavage in PS II core complexes from spinach. FEBS Lett. 378:1996;140-144.
50. + in PS II membrane fragments from spinach. Photosynth. Res. 22:1989;247-256.
51. Fersht A. W. H. Enzyme Structure and Mechanism. 1985;Freeman, New York.
52. Cleland W.W. Low barrier hydrogen bonds in enzymatic catalysis. Arch. Biochem. Biophys. 382:2000;1-5.
53. Northrop D.B. Follow the protons: a low-barrier hydrogen bond unifies the mechanisms of the aspartic proteases. Acc. Chem. Res. 34:2001;790-797.
54. Smedarchina Z., Siebrand W., Fernandez-Ramos A., Cui Q. Kinetic isotope effects for concerted multiple proton transfer: a direct dynamics study of an active-site model of carbonic anhydrase II. J. Am. Chem. Soc. 125:2003;243-251.
55. Chen H., Li S., Jiang Y. A density functional theory study on the intramolecular proton transfer in the enzyme carbonic anhydrase. J. Phys. Chem., A. 107:2003;4652-4660.
56. Zundel G. Hydrogen bonds with large proton polarizability and proton-transfer processes in electrochemistry and biology. Prigogine I., Rice S.A. Advances in Chemical Physics. vol. 111:2000;1-219 Wiley, New York.
57. 2 as a chemical switch: a bond order and atoms in molecules study of hydrogen bonding determined by surrounding groups. J. Phys. Chem., A. 106:2002;11221-11226.
58. 2 step. Biochemistry. 41:2002;4117-4126.
59. 1 states of the oxygen-evolving complex. Biochemistry. 42:2003;8066-8076.
60. Renger G., Völker M. Studies on the proton release of the donor side of system II. Correlation between oxidation and deprotonization of donor D1 in Tris-washed inside-out thylakoids. FEBS Lett. 149:1982;203-207.
61. Christophorov L.N., Holzwarth A.R., Kharkyanen V.N., van Mourik F. Structure-function self-organization in nonequilibrium macromolecular systems. Chem. Phys. 256:2000;45-60.
62. Trissl H.-W., Bernhard K., Lapin M. Evidence for protein dielectric relaxations in reaction centers associated with the primary charge separation detected from Rhodospirillum rubrum chromatophores by combined photovoltage and absorption measurements in the 1-15 ns time range. Biochemistry. 40:2001;5290-5298.
63. 559 complex at 77 K. J. Phys. Chem., B. 101:1997;2933-2944.
64. Vasilev S., Lee C.-I., Brudvig G.W., Bruce D. Structure-based kinetic modeling of excited-state transfer and trapping in histidine-tagged Photosystem II core complexes from Synechocystis. Biochemistry. 41:2002;12236-12243.
65. Mulkidjanian A. Photosystem II of green plants: on the possible role of retarded protonic relaxation in water oxidation. Biochim. Biophys. Acta. 1999;1-6.
66. + reduction during water splitting. Biochemistry. 37:1998;3974-3981.
67. +· reduction in Photosystem II with an intact water oxidising complex. FEBS Lett. 429:1998;49.
68. + in oxygen-evolving photosystem II particles from Chlamydomonas. Biochemistry. 41:2002;15754-15761.
69. Babcock G.T. The oxygen-evolving complex in photosystem II as a metallo-radical enzyme. Mathis P. Photosynthesis: From Light to Biosphere. 1995;209-215 Kluwer Academic Publishing, Dordrecht.
70. Rappaport F., Lavergne J. Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim. Biophys. Acta. 1503:2001;246-259.
71. Junge W., Haumann M., Ahlbrink R., Mulkidjanian A., Clausen J. Electrostatics and proton transfer in photosynthetic water oxidation. Philos. Trans. R. Soc. Lond. B. 357:2002;1407-1418.
72. Tommos C. Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation. Philos. Trans. R Soc. Lond., B. 357:2002;1383-1394.
73. Yachandra V.K. Structure of the manganese complex in photosystem II: insights from X-ray spectroscopy. Philos. Trans. R. Soc. Lond., B. 35z7:2002;1347-1358.
74. 2. Biggins J. Progr. Photosynth. Res. vol. 1:1987;545-548 Martinus Nijhoff/Dr. W. Junk, Dordrecht.
75. +-reduction, fluorescence induction and oxygen evolution in PS II-membrane fragments from spinach. Biochim. Biophys. Acta. 890:1987;66-77.
76. Z in calcium-depleted Photosystem II. Biochim. Biophys. Acta. 1411:1999;121-133.
77. Olesen K., Andreasson L.-E. The function of the chloride ion in photosynthetic oxygen evolution. Biochemistry. 42:2003;2025-2035.
78. Z in PS II core complexes from spinach. Proc. 12th Int. Congr. Photosynthesis, Brisbane S13-024. 2001;. www.publish.csiro.au/ps.
79. + channel. Photosynth. Res. 65:2000;141-154.
80. Laberge M., Huang Q., Schweitzer-Stenner R., Fidy J. The endogenous calcium ions of horseradish peroxidase C are required to maintain the functional nonplanarity of the heme. Biophys. J. 84:2003;2542-2552.
81. Babcock G.T., Blankenship R.E., Sauer K. Reaction kinetics for positive charge accumulation on the water side of chloroplast photosystem II. FEBS Lett. 61:1976;286-289.
82. Dekker J.P., Plijter J.J., Ouwehand L., van Gorkom H.J. Kinetics of manganese redox transitions in the oxygen-evolving apparatus of photosynthesis. Biochim. Biophys. Acta. 767:1984;176-179.
83. Renger G., Weiss W. Functional and structural aspects of photosynthetic water oxidation. Biochem. Soc. Trans. 14:1986;17-20.
84. Rappaport F., Blanchard-Desce M., Lavergne J. Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen evolving complex. Biochim. Biophys. Acta. 1184:1994;178-192.
85. van Leeuwen P.J., Heimann C., Gast P., Dekker J.P., van Gorkom H.J. Flash-induced redox changes in oxygen evolving spinach Photosystem II core particles. Photosynth. Res. 38:1993;169-176.
86. Razeghifard M.R., Pace R.J. Electron paramagnetic resonance kinetic studies of the S states in spinach PS II membranes. Biochim. Biophys. Acta. 1322:1997;141-150.
87. Koike H., Hanssum B., Inoue Y., Renger G. Temperature dependence of S-state transition in a thermophilic cyanobacterium, Synechococcus vulcanus Copeland, measured by absorption changes in UV region. Biochim. Biophys. Acta. 893:1987;524-533.
88. Renger G., Hanssum B. Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett. 299:1992;28-32.
89. 0. Ber. Bunsenges. Phys. Chem. 100:1996;1987-1992.
90. 2O. Biochemistry. 36:1997;8904-8913.
91. Z radical in oxygen evolving and tris-washed photosystem II membranes by time resolved EPR. Biochim. Biophys. Acta. 1322:1997;129-140.
92. Renger G. Studies on structure and mechanism of photosynthetic water oxidation. Peschek G.A., Löffelhardt W., Schmetter G. The Phototrophic Prokaryotes. 1999;35-50 Plenum, New York.
93. Page C.C., Moser C.C., Chen X., Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature. 402:1999;47-52.
94. Tommos C., Babcock G.T. Proton and hydrogen currents in photosynthetic water oxidation. Biochim. Biophys. Acta. 1458:2000;199-219.
95. · in PS II membranes - evidence for concerted hydrogen-atom transfer in oxygen evolution. Biochemistry. 39:2000;16220-16229.
96. 3 transition: implications for the mechanism of photosynthetic water oxidation. J. Am. Chem. Soc. 123:2001;7804-7820.
97. Goussias C., Boussac A., Rutherford A.W. Photosystem II and photosynthetic oxidation of water: an overview. Philos. Trans. R. Soc. Lond., B. 357:2002;1369-1381.
98. Lavergne J., Junge W. Proton release during the redox cycle of the water oxidase. Photosynth. Res. 38:1993;279-296.
99. Haumann M., Junge W. Protons and charge indicators in oxygen evolution. Ort D.R., Yocum C.F. Oxygenic Photosynthesis: The Light Reactions. 1996;165-192 Kluwer Academic Publishing, Dordrecht.
100. Renger G. Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim. Biophys. Acta. 1503:2001;210-228.
101. Vrettos J.S., Brudvig G.W. Water oxidation chemistry of photosystem II. Philos. Trans. R. Soc. Lond., B. 357:2002;1395-1405.
102. Wikström M., Verkhovsky M.I., Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta. 1604:2003;61-65.
103. 2 evolving complex of photosystem II vary independently during S-state turnover. Biochemistry. 39:2000;4399-4405.
104. Renger G. Theoretical studies about the functional and structural organization of photosynthetic oxygen evolution. Metzner H. Photosynthetic Oxygen Evolution. 1978;229-248 Academic Press, London.
105. Krishtalik L.I. Energetics of multielectron reactions. Photosynthetic oxygen evolution. Biochim. Biophys. Acta. 849:1986;162-171.
106. Kaim W., Schwederski B. Bioinorganic Chemistry: Inorganic Elements in the Chemistry of Life: An Introduction and Guide (Inorg. Chemistry). 1995;Wiley.
107. 0 transition. Biochemistry. 38:1999;1252-1257.
108. Maliekal J., Karapetian A., Vance C., Yikilmaz E., Wu Q., Jackson T., Brunold T.C., Spiro T.G., Miller A.-F. Comparison and contrasts between the active site pKs of Mn-superoxide dismutase and those of Fe-superoxide dismutase. J. Am. Chem. Soc. 124:2002;15064-15075.
109. 13C isotope labeling. Biochemistry. 42:2003;6035-6042.
110. Wentworth P., Jones L.H., Wentworth A.D., Zhu X.Y., Larsen N.A., Wilson I.A., Xu X., Goddard W.A., Janda K.D., Eschenmoser A., Lerner R.A. Antibody catalysis of the oxidation of water. Science. 293:2001;1806-1811.
111. Datta D., Vaidehi N., Xu X., Goddard W.A. Mechanism for antibody catalysis of the oxidation of water by singlet dioxygen. Proc. Natl. Acad. Sci. U. S. A. 99:2002;2636-2641.
112. Wentworth P. Jr., Wentworth A.D., Zhu X., Wilson I.A., Janda K.D., Eschenmoser A., Lerner R.A. Evidence for the production of trioxygen species during antibody-catalyzed chemical modification of antigens. Proc. Natl. Acad. Sci. U. S. A. 100:2003;1490-1493.
113. Higuchi M., Noguchi T., Sonoike K. Over-reduced states of the Mn-cluster in cucumber leaves induced by dark-chilling treatment. Biochim. Biophys. Acta. 1604:2003;151-158.
114. Schmidt B., McCracken J., Ferguson-Miller S. A discrete water exit pathway in the membrane protein cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 100:2003;15539-15542.
115. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. U. S. A. 100:2003;15304-15309.