Current Models and Mechanism of Water Splitting

Photosynthetic Protein Complexes: A Structural Approach

Volumn , Issue , 2008, Pages 107-136

  Mccarrick, Robert M ^a   Britt, R David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Babcock model; Brudvig Pecoraro mechanisms for water oxidation; Dangler structure; Hydrogen atom abstraction model; Messinger mechanism; Monomer trimer structure; OEC structure, water binding release; Water oxidation mechanisms; Water splitting

Indexed keywords

EID: 77955239344     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527623464.ch5     Document Type: Chapter

References (110)

1. Blankenship, R.E. (2006) Photosynthesis: the light reactions, in Plant Physiology, 4th edn (ed Lincoln Taiz, Eduardo Zeiger), Sinauer Associates, pp. 125-58.
2. Barber, J. (2003) Photosystem II: the engine of life. Quarterly Reviews of Biophysics, 36, 71-89.
3. Bricker, T.M. and Ghanotakis, D.F. (1996) Introduction to oxygen evolution and the oxygen-evolving complex. Advances in Photosynthesis, 4, 113-36.
4. Britt, R.D. (1996) Oxygen evolution. Advances in Photosynthesis, 4, 137-64.
5. Nelson, N. and Yocum, C.F. (2006) Structure and function of photosystems I and II. Annual Review of Plant Biology, 57, 521-65.
6. Joliot, P., Barbieri, G. and Chabaud, R. (1969) Model of the System II photochemical centers. Photochemistry and Photobiology, 10, 309-29.
7. Kok, B., Forbush, B. and McGloin, M. (1970) Cooperation of charges in photosynthetic oxygen evolution. I. A linear four step mechanism. Photochemistry and Photobiology, 11, 457-75.
8. Babcock, G.T., Barry, B.A., Debus, R.J., Hoganson, C.W., Atamian, M., McIntosh, L., Sithole, I. and Yocum, C.F. (1989) Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. Biochemistry, 28, 9557-65.
9. Debus, R.J. (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochimica et Biophysica Acta, Bioenergetics, 1102, 269-352.
10. Pirson, A. (1937) A study of the nutrition and metabolism of Fontinalis and Chlorella. Zeitschrift fuer Botanik, 31, 193-267.
11. Kessler, E. (1955) On the role of manganese in the oxygen-evolving system of photosynthesis. Archives of Biochemistry and Biophysics, 59, 527-9.
12. Astier, C., Styring, S., Maison-Peteri, B. and Etienne, A.L. (1986) Preparation and characterization of thylakoid membranes and photosystem II particles from the facultative phototrophic cyanobacterium Synechocystis 6714. Photobiochemistry and Photobiophysics, 11, 37-47.
13. Ghanotakis, D.F., Demetriou, D.M. and Yocum, C.F. (1987) Isolation and characterization of an oxygen-evolving photosystem II reaction center core preparation and a 28 kDa Chl-a-binding protein. Biochimica et Biophysica Acta, Bioenergetics, 891, 15-21.
14. Yamada, Y., Tang, X.S., Ito, S. and Sato, K. (1987) Purification and properties of an oxygen-evolving photosystem II reaction-center complex from spinach. Biochimica et Biophysica Acta, Bioenergetics, 891, 129-37.
15. Ghanotakis, D.F., Topper, J.N. and Yocum, C.F. (1984) Structural organization of the oxidizing side of photosystem II. Exogenous reductants reduce and destroy the manganese complex in photosystems II membranes depleted of the 17-and 23-kDa polypeptides. Biochimica et Biophysica Acta, Bioenergetics, 767, 524-31.
16. Ghanotakis, D.F., Babcock, G.T. and Yocum, C.F. (1984) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted photosystem II preparations. FEBS Letters, 167, 127-30.
17. Homann, P.H. (1988) Structural effects of chloride and other anions on the water oxidizing complex of chloroplast photosystem II. Plant Physiology, 88, 194-9.
18. Ono, T., Nakayama, H., Gleiter, H., Inoue, Y. and Kawamori, A. (1987) Modification of the properties of S2 state in photosynthetic O2-evolving center by replacement of chloride with other anions. Archives of biochemistry and biophysics, 256, 618-24.
19. Kelley, P.M. and Izawa, S. (1978) The role of chloride ion in photosystem II. I. Effects of chloride ion on photosystem II electron transport and on hydroxylamine inhibition. Biochimica et Biophysica Acta, Bioenergetics, 502, 198-210.
20. Sandusky, P.O. and Yocum, C.F. (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. Biochimica et Biophysica Acta, Bioenergetics, 766, 603-11.
21. Dismukes, G.C. and Siderer, Y. (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proceedings of the National Academy of Sciences of the United States of America, 78, 274-8.
22. Dismukes, G.C. and Siderer, Y. (1980) EPR spectroscopic observations of a manganese center associated with water oxidation in spinach chloroplasts. FEBS Letters, 121, 78-80.
23. Reed, G.H. and Markham, G.D. (1984) EPR of manganese(II) complexes with enzymes and other proteins. Biological Magnetic Resonance, 6, 73-142.
24. Law, N.A., Caudle, M.T. and Pecoraro, V.L. (1998) Manganese redox enzymes and model systems: properties, structures, and reactivity, Advances in Inorganic Chemistry, 46, 305-440.
25. Cooper, S.R., Dismukes, G.C., Klein, M.P. and Calvin, M. (1978) Mixed valence interactions in di-m-oxo bridged manganese complexes. Electron paramagnetic resonance and magnetic susceptibility studies. Journal of the American Chemical Society, 100, 7248-52.
26. Mukhopadhyay, S., Mandal, S.K., Bhaduri, S. and Armstrong, W.H. (2004) Manganese clusters with relevance to Photosystem II. Chemical Reviews (Washington, DC, United States), 104, 3981-4026.
27. Kirby, J.A., Robertson, A.S., Smith, J.P., Thompson, A.C., Cooper, S.R. and Klein, M.P. (1981) State of manganese in the photosynthetic apparatus. 1. Extended x-ray absorption fine structure studies on chloroplasts and di-m-oxo -bridged dimanganese model compounds. Journal of the American Chemical Society, 103, 5529-37.
28. Penner-Hahn, J.E. (2004) X-ray absorption spectroscopy. Comprehensive Coordination Chemistry II, 2, 159-86.
29. Kirby, J.A., Goodin, D.B., Wydrzynski, T., Robertson, A.S. and Klein, M.P. (1981) State of manganese in the photosynthetic apparatus. 2. X-ray absorption edge studies on manganese in photosynthetic membrane. Journal of the American Chemical Society, 103, 5537-42.
30. Ghanotakis, D.F., Babcock, G.T. and Yocum, C.F. (1984) Structural and catalytic properties of the oxygen -evolving complex. Correlation of polypeptide and manganese release with the behavior of Z+ in chloroplasts and a highly resolved preparation of the PS II complex. Biochimica et Biophysica Acta, Bioenergetics, 765, 388-98.
31. Berthold, D.A., Babcock, G.T. and Yocum, C.F. (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron-transport properties. FEBS Letters, 134, 231-4.
32. Yachandra, V.K., Guiles, R.D., McDermott, A., Britt, R.D., Dexheimer, S.L., Sauer, K. and Klein, M.P. (1986) The state of manganese in the photosynthetic apparatus. 4. Structure of the manganese complex in photosystem II studied using EXAFS spectroscopy. The S1 state of the oxygen-evolving photosystem II complex from spinach. Biochimica et Biophysica Acta, Bioenergetics, 850, 324-32.
33. George, G.N., Prince, R.C. and Cramer, S.P. (1989) The manganese site of the photosynthetic water-splitting enzyme. Science (Washington, DC, United States), 243, 789-91.
34. Yachandra, V.K., DeRose, V.J., Latimer, M.J., Mukerji, I., Sauer, K. and Klein, M.P. (1993) Where plants make oxygen: a structural model for the photosynthetic oxygen-evolving manganese cluster. Science (Washington, DC, United States), 260, 675-9.
35. Zimmermann, J.L. and Rutherford, A.W. (1986) Electron paramagnetic resonance properties of the S2 state of the oxygen -evolving complex of photosystem II. Biochemistry, 25, 4609-15.
36. Zimmermann, J.L. and Rutherford, A.W. (1984) EPR studies of the oxygen-evolving enzyme of photosystem II. Biochimica et Biophysica Acta, Bioenergetics, 767, 160-7.
37. Casey, J.L. and Sauer, K. (1984) EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. Biochimica et Biophysica Acta, Bioenergetics, 767, 21-8.
38. Kim, D.H., Britt, R.D., Klein, M.P. and Sauer, K. (1992) The manganese site of the photosynthetic oxygen-evolving complex probed by EPR spectroscopy of oriented photosystem II membranes: the g = 4 and g = 2 multiline signals. Biochemistry, 31, 541-7.
39. Haddy, A., Lakshmi, K.V., Brudvig Gary, W., Harry, F. and A. (2004) Q-band EPR of the S2 state of photosystem II confirms an S = 5/2 origin of the X-band g = 4.1 signal. Biophysical Journal, 87, 2885-96.
40. Astashkin, A.V., Kodera, Y. and Kawamori, A. (1994) Pulsed EPR study of manganese g = 4.1 signal in plant photosystem II, Journal of Magnetic Resonance, Series B, 105, 113-9.
41. Force, D.A., Randall, D.W., Lorigan, G.A., Clemens, K.L. and Britt, R.D. (1998) ESEEM studies of alcohol binding to the manganese cluster of the oxygen evolving complex of photosystem II. Journal of the American Chemical Society, 120, 13321-33.
42. Boussac, A., Girerd, J.-J. and Rutherford, A.W. (1996) Conversion of the spin state of the manganese complex in Photosystem II induced by Near-Infrared Light. Biochemistry, 35, 6984-9.
43. Messinger, J., Robblee, J., Yu, W.O., Sauer, K., Yachandra, V.K. and Klein, M.P. (1997) The S0 state of the oxygen -evolving complex in photosystem II is paramagnetic: detection of an EPR multiline signal. Journal of the American Chemical Society, 119, 11349-50.
44. Messinger, J., Nugent, J.H. and Evans, M.C.W. (1997) Detection of an EPR multiline signal for the S0 state in photosystem II. Biochemistry, 36, 11055-60.
45. Kulik, L.V., Lubitz, W. and Messinger, J. (2005) Electron spin-lattice relaxation of the S0 state of the oxygen-evolving complex in Photosystem II and of dinuclear manganese model complexes. Biochemistry, 44, 9368-74.
46. Kulik, L.V., Epel, B., Lubitz, W. and Messinger, J. (2005) 55Mn pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in Photosystem II. Journal of the American Chemical Society, 127, 2392-3.
47. Dexheimer, S.L. and Klein, M.P. (1992) Detection of a paramagnetic intermediate in the S1 state of the photosynthetic oxygen-evolving complex. Journal of the American Chemical Society, 114, 2821-6.
48. Yamauchi, T., Mino, H., Matsukawa, T., Kawamori, A. and Ono, T.-A. (1997) Parallel polarization electron paramagnetic resonance studies of the S1-state manganese cluster in the photosynthetic oxygen-evolving system. Biochemistry, 36, 7520-6.
49. Campbell, K.A., Gregor, W., Pham, D.P., Peloquin, J.M., Debus, R.J. and Britt, R.D. (1998) The 23 and 17 kDa extrinsic proteins of Photosystem II modulate the magnetic properties of the S1-State manganese cluster. Biochemistry, 37, 5039-45.
50. Campbell, K.A., Peloquin, J.M., Pham, D.P., Debus, R.J. and Britt, R.D. (1998) Parallel polarization EPR detection of an S1-State \ " Multiline\ " EPR signal in Photosystem II particles from synechocystis sp. PCC 6803. Journal of the American Chemical Society, 120, 447-8.
51. Hsieh, W.-Y., Campbell Kristy, A., Gregor, W., David Britt, R., Yoder Derek, W., Penner-Hahn James, E. and Pecoraro Vincent, L. (2004) The first spectroscopic model for the S1 state multiline signal of the OEC. Biochimica et Biophysica Acta, 1655, 149-57.
52. Zheng, M. and Dismukes, G.C. (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. Inorganic Chemistry, 35, 3307-19.
53. Hasegawa, K., Ono, T., Inoue, Y. and Kusunoki, M. (1999) Spin-exchange interactions in the S2-state manganese tetramer in photosynthetic oxygen -evolving complex deduced from g = 2 multiline EPR signal. Chemical Physics Letters, 300, 9-19.
54. 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. B iochemistry, 37, 9457-65.
55. Aahrling, K.A. and Pace, R.J. (1995) Simulation of the S2 state multiline electron paramagnetic resonance signal of Photosystem II: a multifrequency approach. Biophysical Journal, 68, 2081-2090.
56. Lakshmi, K.V., Eaton, S.S., Eaton, G.R. and Brudvig, G.W. (1999) Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of Photosystem II: an EPR study of the S2YZ.bul. state in oriented acetate-inhibited Photosystem II membranes. Biochemistry, 38, 12758-67.
57. Peloquin, J.M., Campbell, K.A., Randall, D.W., Evanchik, M.A., Pecoraro, V.L., Armstrong, W.H. and Britt, R.D. (2000) 55Mn ENDOR of the S2-state multiline EPR signal of Photosystem II: implications on the structure of the tetranuclear Mn cluster. Journal of the American Chemical Society, 122, 10926-42.
58. Zouni, A., Witt, H.-T., Kern, J., Fromme, P., Krauss, N., Saenger, W. and Orth, P. (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8.ANG. resolution. Nature (London), 409, 739-43.
59. Kamiya, N. and Shen, J.-R. (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 -A resolution. Proceedings of the National Academy of Sciences of the United States of America, 100, 98-103.
60. Ferreira, K.N., Iverson, T.M., Maghlaoui, K., Barber, J. and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science (Washington, DC, United States), 303, 1831-8.
61. 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. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proceedings of the National Academy of Sciences of the United States of America, 102, 12047-52.
62. Cinco Roehl, M., Robblee John, H., Messinger, J., Fernandez, C., McFarlane Holman Karen, L., Sauer, K. and Yachandra Vittal, K. (2004) Orientation of calcium in the Mn4Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of photosystem II membranes. Biochemistry, 43, 13271-82.
63. Cinco, R.M., Robblee, J.H., Rompel, A., Fernandez, C., Visser, H., Messinger, J., McFarlane, K., YachAndra, V.K., Sauer, K. and Klein, M.P. (2000) Structure of the calcium cofactor in oxygen evolution probed by polarized strontium EXAFS on oriented photosystem II membranes, Book of Abstracts, 219th ACS National Meeting (March 26-30, 2000), INOR-064, San Francisco, CA.
64. Yano, J., Kern, J., Sauer, K., Latimer, M.J., Pushkar, Y., Biesiadka, J., Loll, B., Saenger, W., Messinger, J., Zouni, A. and Yachandra, V.K. (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca Cluster. Science (Washington, DC, United States), 314, 821-5.
65. Sproviero, E.M., Gascon, J.A., McEvoy, J.P., Brudvig, G.W. and Batista, V.S. (2006) QM/MM models of the O2 -evolving complex of Photosystem II. Journal of Chemical Theory and Computation, 2, 1119-34.
66. Sproviero, E.M., Gascon, J.A., McEvoy, J.P., Brudvig, G.W. and Batista, V.S. (2006) 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. Journal of Inorganic Biochemistry, 100, 786-800.
67. McEvoy, J.P., Gascon, J.A., Batista, V.S. and Brudvig, G.W. (2005) The mechanism of photosynthetic water splitting. Photochemical and Photobiological Sciences, 4, 940-9.
68. Pecoraro, V.L., Baldwin, M.J., Caudle, M.T., Hsieh, W.-Y. and Law, N.A. (1998) A proposal for water oxidation in photosystem II. Pure and Applied Chemistry, 70, 925-9.
69. Siegbahn, P.E. and Lundberg, M. (2005) The mechanism for dioxygen formation in PSII studied by quantum chemical methods. Photochemical and Photobiological Sciences, 4, 1035-43.
70. Riggs, P.J., Yocum, C.F., Penner-Hahn, J.E. and Mei, R. (1992) Reduced derivatives of the manganese cluster in the photosynthetic oxygen-evolving complex. Journal of the American Chemical Society, 114, 10650-1.
71. Zheng, M. and Dismukes, G.C. (1992) Photosynthetic water oxidation: what have we learned from the multiline EPR signals? Research in Photosynthesis, Vol II (ed. N. Murata), Kluwer Academic Publ., Dordrecht, pp. 305-8.
72. Yachandra, V.K., Guiles, R.D., McDermott, A.E., Cole, J.L., Britt, R.D., Dexheimer, S.L., Sauer, K. and Klein, M.P. (1987) Comparison of the structure of the manganese complex in the S1 and S2 states of the photosynthetic O2-evolving complex: an x-ray absorption spectroscopy study. Biochemistry, 26, 5974-81.
73. Iuzzolino, L., Dittmer, J., Dorner, 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, 17112-19.
74. Roelofs, T.A., Liang, W., Latimer, M.J., Cinco, R.M., Rompel, A., andrews, J.C., Sauer, K., YachAndra, V.K. and Klein, M.P. (1996) Oxidation states of the manganese cluster during the flash -induced S-state cycle of the photosynthetic oxygen-evolving complex. Proceedings of the National Academy of Sciences of the United States of America, 93, 3335-40.
75. Ono, T., Noguchi, T., Inoue, Y., Kusunoki, M., Matsushita, T. and Oyanagi, H. (1992) X-ray-detection of the period-4 cycling of the manganese cluster in photosynthetic water oxidizing enzyme. Science, 258, 1335-7.
76. Messinger, J., Robblee, J.H., Bergmann, U., Fernandez, C., Glatzel, P., Visser, H., Cinco, R.M., McFarlane, K.L., Bellacchio, E., Pizarro, S.A., Cramer, S.P., Sauer, K., Klein, M.P. and Yachandra, V.K. (2001) Absence of Mn-centered oxidation in the S2-> S3 transition: implications for the mechanism of photosynthetic water oxidation. Journal of the American Chemical Society, 123, 7804-20.
77. Hallahan, B.J., Nugent, J.H.A., Warden, J.T. and Evans, M.C.W. (1992) Investigation of the origin of the \ " S3\ " EPR signal from the oxygen-evolving complex of photosystem 2: the role of tyrosine Z. Biochemistry, 31, 4562-73.
78. Ioannidis, N., Nugent, J.H. and Petrouleas, V. (2002) Intermediates of the S3 state of the oxygen-evolving complex of Photosystem II. Biochemistry, 41, 9589-600.
79. Geijer, P., Morvaridi, F. and Styring, S. (2001) The S3 state of the oxygen -evolving complex in Photosystem II Is converted to the S2YZ.bul. State at Alkaline pH. Biochemistry, 40, 10881-91.
80. Ioannidis, N. and Petrouleas, V. (2000) Electron paramagnetic resonance signals from the S3 state of the oxygen-evolving complex. A broadened radical signal induced by low-temperature near-infrared light illumination. Biochemistry, 39, 5246-54.
81. Boussac, A. and Rutherford, A.W. (1992) The origin of the split S3 EPR signal in calcium-depleted photosystem II: histidine versus tyrosine. Biochemistry, 31, 7441-5.
82. Dekker, J.P., Van Gorkom, H.J., Wensink, J. and Ouwehand, L. (1984) Absorbance difference spectra of the successive redox states of the oxygen -evolving apparatus of photosynthesis. Biochimica et Biophysica Acta, Bioenergetics, 767, 1-9.
83. Dekker, J.P., Van Gorkom, H.J., Brok, M. and Ouwehand, L. (1984) Optical characterization of photosystem II electron donors. Biochimica et Biophysica Acta, Bioenergetics, 764, 301-9.
84. Dekker, J.P. (1992) Optical studies on the oxygen-evolving complex of photosystem II. Manganese Redox Enzymes, 85-103.
85. Strickler, M.A., Hillier, W. and Debus, R.J. (2006) No evidence from FTIR difference spectroscopy that glutamate -189 of the D1 polypeptide ligates a Mn ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in Photosystem II. Biochemistry, 45, 8801-11.
86. Kimura, Y. and Ono, T.-a. (2006) Structural and functional studies of photosynthetic oxygen evolving Mn cluster by means of FTIR spectroscopy. Seibutsu Butsuri, 46, 124-9.
87. Debus, R.J., Strickler, M.A., Walker, L.M. and Hillier, W. (2005) No evidence from FTIR difference spectroscopy that Aspartate-170 of the D1 polypeptide ligates a manganese ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in Photosystem II. Biochemistry, 44, 1367-74.
88. Haumann, M., Muller, C., Liebisch, P., Iuzzolino, L., Dittmer, J., Grabolle, M., Neisius, T., Meyer-Klaucke, W. and Dau, H. (2005) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3,4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry, 44, 1894-908.
89. Haumann, M., Liebisch, P., Muller, C., Barra, M., Grabolle, M. and Dau, H. (2005) Photosynthetic O2 formation tracked by time-resolved x-ray experiments. Science, 310, 1019-21.
90. Clausen, J., Junge, W., Dau, H. and Haumann, M. (2005) Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry, 44, 12775-9.
91. Clausen, J. and Junge, W. (2004) Detection of an intermediate of photosynthetic water oxidation, Nature (London, United Kingdom), 430, 480-3.
92. Radmer, R. and Ollinger, O. (1985) Photosynthesis studies using mass spectrometric techniques. Gas Enzymolology: Proceedings of a Symposium, 91-104.
93. Aznar, C.P. and Britt, R.D. (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. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 357, 1359-66.
94. Evans, M.C.W., Nugent, J.H.A., Ball, R.J., Muhiuddin, I. and Pace, R.J. (2004) Evidence for a direct manganese-oxygen ligand in water binding to the S2 state of the photosynthetic water oxidation complex. Biochemistry, 43, 989-94.
95. Hillier, W. and Wydrzynski, T. (2004) Substrate water interactions within the Photosystem II oxygen evolving complex, Physical Chemistry Chemical Physics, 6, 4882-9.
96. 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, 13328-34.
97. Richens, D.T. (2005) Ligand substitution reactions at inorganic centers. Chemical Reviews (Washington, DC, United States), 105, 1961-2002.
98. Helm, L. and Merbach, A.E. (2005) Inorganic and bioinorganic solvent exchange mechanisms. Chemical Reviews (Washington, DC, United States), 105, 1923-59.
99. Hoganson, C.W. and Babcock, G.T. (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science, 277, 1953-6.
100. Schlodder, E. and Witt, H.T. (1999) Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation Reexamination by a glass electrode study at pH 5.5-7.2. Journal of Biological Chemistry, 274, 30387-92.
101. Dau, H. and Haumann, M. (2006) Response to photosynthetic oxygen production. Science (Washington, DC, United States), 312, 1471-2.
102. Haumann, M., Bogershausen, 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. Photosynthesis Research, 51, 193-208.
103. Ahlbrink, R., Haumann, M., Cherepanov, D., Boegershausen, 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, 1131-42.
104. Haumann, M., Mulkidjanian, A. and Junge, W. (1999) Tyrosine-Z in oxygen -evolving Photosystem II: a hydrogen -bonded tyrosinate. Biochemistry, 38, 1258-67.
105. Limburg, J., Szalai, V.A. and Brudvig, G.W. (1999) A mechanistic and structural model for the formation and reactivity of a MnV:O species in photosynthetic water oxidation. Journal of the Chemical Society, Dalton Transactions: Inorganic Chemistry, 1353-62.
106. Britt, R.D., Campbell, K.A., Peloquin, J.M., Gilchrist, M.L., Aznar, C.P., Dicus, M.M., Robblee, J. and Messinger, J. (2004) Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochimica Et Biophysica Acta-Bioenergetics, 1655, 158-71.
107. Haumann, M., Barra, M., Loja, P., Loescher, S., Krivanek, R., Grundmeier, A., andreasson, L.-E. and Dau, H. (2006) Bromide does not bind to the Mn4Ca complex in its S1 state in Cl-depleted and Br-reconstituted oxygen -evolving Photosystem II: evidence from X-ray absorption spectroscopy at the Br K-edge. Biochemistry, 45, 13101-7.
108. Yu, H., Aznar, C.P., Xu, X.Z. and Britt, R.D. (2005) Evidence that azide occupies the chloride binding site near the manganese cluster in photosystem II. Biochemistry, 44, 12022-9.
109. Clemens, K.L., Force, D.A. and Britt, R.D. (2002) Acetate binding at the photosystem II oxygen evolving complex: an S-2-state multiline signal ESEEM study. Journal of the American Chemical Society, 124, 10921-33.
110. Messinger, J. and Renger, G. The Royal Society Chemistry (2008) Photosynthetic water splitting. Primary Processes of Photosynthesis: Basic Principles and Apparatus, Comprehensive Series in Photochemical and Photobiological Sciences, (in press).