Substrate water binding and oxidation in photosystem II

Photosynthesis Research

Volumn 98, Issue 1-3, 2008, Pages 261-276

  McConnell, Iain L ^a,b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b YALE UNIVERSITY   (United States)

Author keywords

Photosystem II; Substrate water; Water exchange; Water oxidation; Water oxidising complex

Indexed keywords

OXYGEN; WATER;

CHEMISTRY; CONFORMATION; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHOTOSYSTEM II; REVIEW;

MOLECULAR CONFORMATION; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; WATER;

EID: 57849167419     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-008-9337-7     Document Type: Review

References (121)

1. N Adir I Ohad 1988 Structural properties of the D1 and surrounding photosystem II polypeptides as revealed by their interaction with cross-linking reagents J Biol Chem 263 283 289
2. 0 state of the oxygen evolving complex in photosystem II Biochemistry 36 13148 13152 10.1021/bi971815w
3. Åhrling KA, Pace RJ, Evans MCW (2005) The catalytic manganese cluster: implications form spectroscopy. In: Wydrzynksi T, Satoh K (eds) Photosystem II-the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 285-305
4. G Ananyev GC Dismukes 2005 How fast can photosystem II split water? Kinetic performance at high and low frequencies Photosynth Res 85 355 365 10.1007/s11120-004-7081-1
5. G Ananyev T Nguyen C Putnam-Evans GC Dismukes 2005 Mutagenesis of CP43-arginine-357 to serine reveals new evidence for (bi)carbonate functioning in the water oxidizing complex of photosystem II Photochem Photobiol Sci 4 991 998 10.1039/b507519j
6. JM Anderson 2001 Does functional photosystem II complex have an oxygen channel? FEBS Lett 488 1 4 10.1016/S0014-5793(00)02358-9
7. A Bekker HD Holland PL Wang D Rumble III HJ Stein JL Hannah 2004 Dating the rise of atmospheric oxygen Nature 427 117 120 10.1038/nature02260
8. DA Berthold GT Babcock CF Yocum 1981 A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes EPR and electron-transport properties FEBS Lett 134 231 234 10.1016/0014-5793(81)80608-4
9. J Biesiadka B Loll J Kern K-D Irrgang A Zouni 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 10.1039/b406989g
10. 4+ J Am Chem Soc 122 8464 8473 10.1021/ja993235n
11. RD Britt KA Campbell JM Peloquin ML Gilchrist CP Aznar MM Dicus 2004 Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms Biochim Biophys Acta 1655 158 171 10.1016/j.bbabio.2003.11.009
12. TG Carell AM Tyryshkin GC Dismukes 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 10.1007/s00775-001- 0305-3
13. HA Chu MT Gardner W Hillier GT Babcock 2000 Low-frequency fourier transform infrared spectroscopy of the oxygen-evolving complex in Photosystem II Photosynth Res 66 57 63 10.1023/A:1010779327960
14. HA Chu H Sackett GT Babcock 2000 Identification of a Mn-O-Mn cluster vibrational mode of the oxygen-evolving complex in photosystem II by low-frequency FTIR spectroscopy Biochemistry 47 14371 14376 10.1021/bi001751g
15. 2 transition: an isotope-edited FTIR study Biochemistry 43 3152 3166 10.1021/bi035915f
16. J Clausen W Junge 2004 Detection of an intermediate of photosynthetic water oxidation Nature 430 480 483 10.1038/nature02676
17. A Cua DH Stewart MJ Reifler GW Brudvig DF Bocian 2000 Low-frequency resonance Raman characterization of the oxygen-evolving complex of photosystem II J Am Chem Soc 122 2069 2077 10.1021/ja9932885
18. H Dau M Haumann 2007 Eight steps preceding O-O bond formation in oxygenic photosynthesis-A basic reaction cycle of the photosystem II manganese complex Biochim Biophys Acta 1767 472 483 10.1016/j.bbabio.2007.02.022
19. H Dau L Iuzzolino J Dittmer 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 10.1016/S0005-2728(00)00230-9
20. H Dau P Leibisch M Haumann 2003 X-ray absorption spectroscopy to analyse nuclear geometry and electronic structure of biological metal centres-potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis Anal Bioanal Chem 376 562 583 10.1007/s00216-003- 1982-2
21. Dau H, Grundmeier A, Loja P, Haumann M (2007) On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomic-resolution models for four S-states. Phil Trans R Soc B Epub ahead of print
22. 2 states of the water oxidizing complex of photosystem II Biochim Biophys Acta 1412 240 249 10.1016/S0005-2728(99)00064-X
23. Debus R (2005) The catalytic manganese cluster: protein ligation. In: Wydrzynski T, Satoh K (eds) Photosystem II-the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 261-284
24. 3 transitions in photosystem II Biochemistry 44 1367 1374 10.1021/bi047558u
25. J Deisenhofer H Michel 1989 The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis EMBO J 8 2149 2170
26. JP Dekker HJ van Gorkom M Brok L Ouwehand 1984 Optical characterization of photosystem II electron donors Biochim Biophys Acta 764 301 309 10.1016/0005-2728(84)90100-2
27. VJ DeRose I Mukerji MJ Latimer VK Yachandra K Sauer MP Klein 1994 Comparison of the manganese oxygen-evolving complex in photosystem II of spinach and Synechococcus sp. with multinuclear manganese model compounds by x-ray absorption spectroscopy J Am Chem Soc 116 5239 5249 10.1021/ja00091a031
28. GC Dismukes Y Siderer 1980 EPR spectroscopic observations of a manganese center associated with water oxidation in spinach chloroplasts FEBS Lett 121 78 80 10.1016/0014-5793(80)81270-1
29. GC Dismukes Y Siderer 1981 Intermediates of a polynuclear manganese cluster involved in photosynthetic oxidation of water Proc Natl Acad Sci USA 78 274 278 10.1073/pnas.78.1.274
30. 2 state FEBS Lett 579 3081 3084 10.1016/j.febslet.2005.04.066
31. KN Ferreira TM Iverson K Maghlaoui J Barber S Iwata 2004 Architecture of the photosynthetic oxygen-evolving center Science 303 1831 1838 10.1126/science.1093087
32. DA Force DW Randall GA Lorigan KL Clemens RD Britt 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 10.1021/ja982713b
33. SW Gersten GJ Samuels TJ Meyer 1982 Catalytic oxidation of water by an oxo-bridged ruthenium dimer J Am Chem Soc 104 4029 4030 10.1021/ja00378a053
34. P Glatzel U Bergmann J Yano H Visser W Gu JH Robblee 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 10.1021/ja038579z
35. DB Goodin VK Yachandra RD Britt K Sauer MP Klein 1984 The state of manganese in the photosynthetic apparatus. 3. Light-induced changes in X-ray absorption (K-edge) energies of manganese in photosynthetic membranes Biochim Biophys Acta 767 209 216 10.1016/0005-2728(84)90189-0
36. M Grabolle M Haumann C Muller P Liebisch H Dau 2006 Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by x-ray irradiation at 10-300 K J Biol Chem 281 4580 4588 10.1074/jbc.M509724200
37. KC Han JR Shen M Ikeuchi Y Inoue 1994 Chemical crosslinking studies of extrinsic proteins in cyanobacterial photosystem II FEBS Lett 355 121 124 10.1016/0014-5793(94)01182-6
38. B Hankamer J Barber EJ Boekema 1997 Structure and membrane organization of photosystem II in green plants Annu Rev Plant Physiol Plant Mol Biol 48 641 671 10.1146/annurev.arplant.48.1.641
39. B Hankamer EP Morris J Barber 1999 Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography Nat Struct Biol 6 560 564 10.1038/9341
40. B Hankamer E Morris J Nield C Gerle J Barber 2001 Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy J Struct Biol 135 262 269 10.1006/jsbi.2001.4405
41. 2 state of photosystem II FEBS Lett 195 151 154 10.1016/0014-5793(86)80150-8
42. 2 formation tracked by time-resolved X-ray experiments Science 310 1019 1021 10.1126/science.1117551
43. 2 state of photosystem II Biochemistry 41 13328 13334 10.1021/bi026246t
44. 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 10.1021/bi034279i
45. W Hillier GT Babcock 2001 Photosynthetic reaction centres Plant Physiol 125 33 37 10.1104/pp.125.1.33
46. Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski T, Satoh K (eds) Photosystem II-the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 567-608
47. 2 evolving mechanism of photosystem II Biochim Biophys Acta 1503 197 209 10.1016/S0005-2728(00)00225-5
48. W Hillier T Wydrzynski 2004 Substrate water interactions within the photosystem II oxygen evolving complex Phys Chem Chem Phys 6 4882 4889 10.1039/b407269c
49. 3 state of photosystem II Biochemistry 37 16908 16914 10.1021/bi980756z
50. W Hillier G Hendry RL Burnap T Wydrzynski 2001 Substrate water exchange in photosystem II depends on the peripheral proteins J Biol Chem 276 46917 46924 10.1074/jbc.M102954200
51. 4 cluster in photosystem II based on solvent accessibility simulations, with implications for substrate water access Biochim Biophys Acta 1777 140 153 10.1016/j.bbabio.2007.08.009
52. CW Hoganson GT Babcock 1997 A metalloradical mechanism for the generation of oxygen from water in photosynthesis Science 277 1953 1956 10.1126/science.277.5334.1953
53. AR Holzwarth MG Müller M Reus M Nowaczyk J Sander M Rögner 2006 Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor Proc Natl Acad Sci USA 103 6895 6900 10.1073/pnas.0505371103
54. JK Hurst 2005 Water oxidation catalyzed by dimeric μ-oxo bridged ruthenium diimine complexes Coord Chem Rev 249 313 328 10.1016/j.ccr.2004.06.017
55. 4+ Ion Inorg Chem 31 1010 1017 10.1021/ic00032a017
56. H Ishikita W Saenger B Loll J Biesiadka E-W Knapp 2006 Energetics of a possible proton exit pathway for water oxidation in photosystem II Biochemistry 45 2063 2071 10.1021/bi051615h
57. 3 transitions of the water oxidation cycle Biochemistry 37 17112 17119 10.1021/bi9817360
58. + reduction in oxygen evolving photosystem II Biochemistry 41 5015 5023 10.1021/bi0118862
59. P Joliot IG Barbier R Chabaud 1969 Un nouveau modele des centres photochimique du systeme II Photochem Photobiol 10 309 329 10.1111/j.1751-1097. 1969.tb05696.x
60. Y Kashino WM Lauber JA Carroll Q Wang J Whitmarsh K Satoh 2002 Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides Biochemistry 41 8004 8012 10.1021/bi026012+
61. Y Kimura A Ishii T Yamanari T-A Ono 2005 Water-sensitive low-frequency vibrations of reaction intermediates during S-state cycling in photosynthetic water oxidation Biochemistry 44 7613 7622 10.1021/bi048203d
62. 2 evolution-I. A linear four step mechanism Photochem Photobiol 11 457 475 10.1111/j.1751-1097.1970.tb06017.x
63. 2 states of the oxygen-evolving complex in photosystem II J Am Chem Soc 127 2392 2393 10.1021/ja043012j
64. 55Mn-ENDOR and EPR spectroscopy J Am Chem Soc 129 13421 13435 10.1021/ja071487f
65. 3 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 10.1021/ja992501u
66. V=O species in photosynthetic water oxidation. J Chem Soc Dalton Trans 1353-1362. doi: 10.1039/a807583b
67. 3 (terpy = 2,2′:6, 2″-terpyridine) J Am Chem Soc 123 423 430 10.1021/ja001090a
68. B Loll J Kern W Saenger A Zouni J Biesiadka 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 1040 1044 10.1038/nature04224
69. M Lundberg PEM Siegbahn 2004 Theoretical investigations of structure and mechanism of the oxygen-evolving complex in PSII Phys Chem Chem Phys 6 4772 4780 10.1039/b406552b
70. J McEvoy G Brudvig 2006 Water-splitting chemistry of photosystem II Chem Rev 106 4455 4483 10.1021/cr0204294
71. xCa structures for the catalytic site and spectroscopic data Phys Chem Chem Phys 6 4764 4771 10.1039/b406437b
72. Messinger J, Renger G (2007) Photosynthetic water splitting. In: Renger G (ed) Primary processes of photosynthesis: basic principles and apparatus, vol II: reaction centers/photosystems, electron transport chains, photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 28-32
73. 3 state of photosystem II Proc Natl Acad Sci USA 92 3209 3213 10.1073/pnas.92.8.3209
74. 0 state of the oxygen-evolving complex in photosystem II is paramagnetic: detection of an EPR multiline signal J Am Chem Soc 119 11349 11350 10.1021/ja972696a
75. -3 state of the water oxidase in photosystem II Biochemistry 36 6862 6873 10.1021/bi962653r
76. J Messinger JH Robblee U Bergmann C Fernandez P Glatzel H Visser 2001 Absence of Mn-centered oxidation in the S2→S3 transition: implications for the mechanism of photosynthetic water oxidation J Am Chem Soc 123 7804 7820 10.1021/ja004307+
77. H Michel J Deisenhofer 1988 Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II Biochemistry 27 1 7 10.1021/bi00401a001
78. JW Murray J Barber 2007 Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel J Struct Biol 159 228 237 10.1016/j.jsb.2007.01.016
79. JF Nagle HJ Morowitz 1978 Molecular mechanisms for proton transport in membranes Proc Natl Acad Sci USA 75 298 302 10.1073/pnas.75.1.298
80. O Nanba K Satoh 1987 Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559 Proc Natl Acad Sci USA 84 109 112 10.1073/pnas.84.1.109
81. T Noguchi 2008 FTIR detection of water reactions in the oxygen-evolving centre of photosystem II Philos Trans R Soc Lond B Biol Sci 363 1189 1195 10.1098/rstb.2007.2214
82. T Noguchi M Sugiura 2000 Structure of an active water molecule in the water-oxidizing complex of photosystem II as studied by FTIR spectroscopy Biochemistry 39 10943 10949 10.1021/bi001040i
83. T Noguchi M Sugiura 2002 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 10.1021/bi011954k
84. T Noguchi M Sugiura 2002 FTIR detection of water reactions during the flash-induced s-state cycle of the photosynthetic water-oxidizing complex Biochemistry 41 15706 15712 10.1021/bi020603i
85. JM Olson RE Blankenship 2004 Thinking about the evolution of photosynthesis Photosynth Res 80 373 386 10.1023/B:PRES.0000030457.06495.83
86. Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh WY, Law NA (1998) A proposal for water oxidation in photosystem II. Pure Appl Chem 70:925. doi: 10.1351/pac199870040925
87. 2 state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster J Am Chem Soc 122 10926 10942 10.1021/ja002104f
88. M Petřek M Otyepka P Banáš P Košinová J Kočal J Damborský 2006 CAVER: a new tool to explore routes from protein clefts, pockets and cavities BMC Bioinformatics 7 316 10.1186/1471-2105-7-316
89. - FEBS Lett 110 57 61 10.1016/0014-5793(80)80022-6
90. F Rappaport M Blanchard-Desce J Lavergne 1994 Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex Biochim Biophys Acta 1184 178 192 10.1016/0005-2728(94)90222-4
91. MR Razeghifard RJ Pace 1998 Electron paramagnetic resonance kinetic studies of the S states in spinach PSII membranes Biochim Biophys Acta 1322 141 150
92. JH Robblee RM Cinco VK Yachandra 2001 X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution Biochim Biophys Acta 1503 7 23 10.1016/S0005-2728(00)00217-6
93. 2 moieties in the tetranuclear Mn complex? J Am Chem Soc 124 7459 7471 10.1021/ja011621a
94. M Rögner EJ Boekema J Barber 1996 How does photosystem 2 split water? The structural basis of efficient energy conversion Trends Biochem Sci 21 44 49
95. 6+: a molecular mimic of the photosynthetic water oxidation enzyme? J Am Chem Soc 122 10353 10357 10.1021/ja0005587
96. K Satoh T Ohno S Katoh 1985 An oxygen-evolving complex with a simple subunit structure-'a water-plastoquinone oxidoreductase'-from the thermophilic cyanobacterium Synechococcus sp FEBS Lett 180 326 330 10.1016/0014-5793(85) 81096-6
97. Satoh K, Wydrzynski T, Govindjee (2005) Introduction to photosystem II. In: Wydrzynksi T, Satoh K (eds) Photosystem II -the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 11-22
98. 4Ca cluster in the water-oxidising complex of photosystem II Photosynth Res 85 73 86 10.1007/s11120-005-0638-9
99. A Seidler 1996 The extrinsic polypeptides of photosystem II Biochim Biophys Acta 1277 35 60 10.1016/S0005-2728(96)00102-8
100. 2 in the presence of water Angew Chem Int Ed 43 98 100
101. S Singh RJ Debus T Wydrzynski W Hillier 2008 Investigation of substrate water interactions at the high-affinity Mn site in the photosystem II oxygen-evolving complex Philos Trans R Soc B 363 1229 1235 10.1098/rstb.2007. 2219
102. 2-evolving complex of photosystem II J Chem Theory Comput 2 1119 1134 10.1021/ct060018l
103. EM Sproviero K Shinopoulos JA Gascon JP McEvoy GW Brudvig VS Batista 2008 QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II Philos Trans R Soc B 363 1149 1156 10.1098/rstb.2007. 2210
104. MA Strickler LM Walker W Hillier RJ Debus 2005 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 44 8571 8577 10.1021/bi050653y
105. 3 transitions in photosystem II Biochemistry 45 8801 8811 10.1021/bi060583a
106. 3 transitions in photosystem II Biochemistry 46 3151 3160 10.1021/bi062195e
107. 4Ca cluster of photosystem II: a preliminary characterization of the Glu354Gln mutant Philos Trans R Soc Lond B Biol Sci 363 1179 1188 10.1098/rstb.2007.2213
108. 17O-HYSCORE spectroscopy J Am Chem Soc 130 786 787 10.1021/ja076620i
109. X-S Tang K Satoh 1984 The oxygen-evolving photosystem II core complex FEBS Lett 179 60 64 10.1016/0014-5793(85)80191-5
110. Thornton LE, Roose JL, Pakrasi HB, Ikeuchi M (2005) The low molecular weight proteins of photosystem II. In: Wydrzynski T, Satoh K (eds) Photosystem {II}-The light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 121-138
111. van Rensen JJS, Klimov VV (2005) Bicarbonate interactions. In: Wydrzynski T, Satoh K (eds) Photosystem II-The light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 329-346
112. JS Vrettos J Limburg GW Brudvig 2001 Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry Biochim Biophys Acta 1503 229 245 10.1016/S0005-2728(00)00214-0
113. 2 formation Biochemistry 40 7937 7945 10.1021/bi010679z
114. 3 state of the oxygen-evolving complex J Am Chem Soc 126 8070 8071 10.1021/ja0494104
115. T Wydrzynski W Hillier J Messinger 1996 On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism Physiol Plant 96 342 350 10.1111/j.1399-3054.1996.tb00224.x
116. Yachandra VK (2005) The catalytic manganese cluster: organization of the metal ions. In: Wydrzynski T, Satoh K (eds) Photosystem II-The light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 235-260
117. VK Yachandra K Sauer MP Klein 1996 Manganese cluster in photosynthesis: where plants oxidize water to dioxygen Chem Rev 96 2927 2950 10.1021/cr950052k
118. 4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography Proc Natl Acad Sci USA 102 12047 12052 10.1073/pnas.0505207102
119. 4Ca cluster J Am Chem Soc 127 14974 14975 10.1021/ja054873a
120. 4Ca cluster Science 314 821 825 10.1126/science.1128186
121. A Zouni HT Witt J Kern P Fromme N Krauss W Saenger 2001 Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution Nature 409 739 743 10.1038/35055589