Evidence from FTIR difference spectroscopy that D1-Asp61 influences the water reactions of the oxygen-evolving Mn4CaO5 cluster of photosystem II

Biochemistry

Volumn 53, Issue 18, 2014, Pages 2941-2955

  Debus, Richard J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN BONDS; MANGANESE; MANGANESE REMOVAL (WATER TREATMENT); MOLECULES; OXIDATION; OXYGEN; PROTONS; REDOX REACTIONS;

COORDINATION SPHERE; ELECTRON-TRANSFER STEP; FTIR DIFFERENCE SPECTROSCOPY; HYDROGEN-BONDED WATER MOLECULES; PHOTOSYNTHETIC WATER OXIDATION; S-STATE TRANSITIONS; SYNECHOCYSTIS SP. PCC 6803; WEAK HYDROGEN BOND;

MANGANESE COMPOUNDS;

BACTERIORHODOPSIN; CALCIUM; CYTOCHROME C OXIDASE; HYDROGEN; MANGANESE; OXYGEN; PROTON; WATER;

ARTICLE; CHLOROPHYLL CONTENT; CRYSTAL STRUCTURE; DARK ADAPTATION; ELECTRON TRANSPORT; HYDROGEN BOND; INDUCED MUTATION; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PHOTOSYSTEM II; POLARIZATION; PRIORITY JOURNAL; PROTON TRANSPORT; SYNECHOCYSTIS; THERMOSYNECHOCOCCUS ELONGATUS; THYLAKOID MEMBRANE;

CALCIUM; CATALYTIC DOMAIN; HYDROGEN BONDING; MANGANESE; PHOTOSYSTEM II PROTEIN COMPLEX; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SYNECHOCYSTIS; WATER;

EID: 84900537962     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500309f     Document Type: Article

References (132)

1. Cardona, T., Sedoud, A., Cox, N., and Rutherford, A. W. (2012) Charge separation in Photosystem II: A comparative and evolutionary overview Biochim. Biophys. Acta 1817, 26-43
2. Barber, J. (2012) Photosystem II: The Water-Splitting Enzyme of Photosynthesis Cold Spring Harbor Symp. Quant. Biol. 77, 295-307
3. Shi, L.-X., Hall, M., Funk, C., and Schröder, W. P. (2012) Photosystem II, a growing complex: Updates on newly discovered components and low molecular mass proteins Biochim. Biophys. Acta 1817, 13-25
4. Vinyard, D. J., Ananyev, G. M., and Dismukes, G. C. (2013) Photosystem II: the reaction center of oxygenic photosynthesis Annu. Rev. Biochem. 82, 577-606
5. 2 Evolution, in Molecular Solar Fuels (Wydrzynski, T. and Hillier, W., Eds.) pp 163-207, Royal Society of Chemistry, Cambridge, UK.
6. Renger, G. (2012) Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms Biochim. Biophys. Acta 1817, 1164-1176
7. Dau, H., Zaharieva, I., and Haumann, M. (2012) Recent developments in research on water oxidation by photosystem II Curr. Opin. Chem. Biol. 16, 3-10
8. Cox, N., Pantazis, D. A., Neese, F., and Lubitz, W. (2013) Biological water oxidation Acc. Chem. Res. 46, 1588-1596
9. Cox, N. and Messinger, J. (2013) Reflections on substrate water and dioxygen formation Biochim. Biophys. Acta 1827, 1020-1030
10. Pokhrel, R. and Brudvig, G. W. (2014) Oxygen-evolving complex of photosystem II: correlating structure with spectroscopy Phys. Chem. Chem. Phys. 10.1039/C4CP00493K
11. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving Photosystem II at a resolution of 1.9 Å Nature 473, 55-60
12. Kawakami, K., Umena, Y., Kamiya, N., and Shen, J.-R. (2011) Structure of the catalytic, inorganic core of oxygen-evolving Photosystem II at 1.9 Å resolution J. Photochem. Photobiol., B 104, 9-18
13. 2-evolving complex of Photosystem II Biochemistry 50, 6308-6311
14. 2 state in the oxygen evolving complex of Photosystem II: protonation states and magnetic interactions J. Am. Chem. Soc. 133, 19743-19757
15. Siegbahn, P. E. M. (2011) The effect of backbone constraints: the case of water oxidation by the oxygen-evolving complex in PSII ChemPhysChem 12, 3274-3280
16. 4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence J. Photochem. Photobiol., B 104, 100-110
17. Galstyan, A., Robertazzi, A., and Knapp, E. W. (2012) Oxygen-evolving Mn cluster in Photosystem II: the protonation pattern and oxidation state in the high-resolution crystal structure J. Am. Chem. Soc. 134, 7442-7449
18. 3 states of oxygen-evolving complex of photosystem II: full geometry optimizations by B3LYP hybrid density functional Dalton Trans. 41, 13727-13740
19. 2 formation in Photosystem II Acc. Chem. Res. 42, 1871-1880
20. 4 cluster of PSII refined to 1.9 Å resolution Chem. Phys. Lett. 511, 138-145
21. 4 transitions in photosystem II Phys. Chem. Chem. Phys. 14, 4849-4856
22. 17O electron-electron double resonance-detected NMR spectroscopy J. Am. Chem. Soc. 134, 16619-16634
23. 2 release Biochim. Biophys. Acta 1827, 1003-1019
24. 3 states J. Am. Chem. Soc. 135, 9442-9449
25. Navarro, M. P., Ames, W. M., Nilsson, H., Lohmiller, T., Pantazis, D. A., Rapatskiy, L., Nowaczyk, M. M., Neese, F., Boussac, A., Messinger, J., Lubitz, W., and Cox, N. (2013) Ammonia binding to the oxygen-evolving complex of photosystem II identified the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer Proc. Natl. Acad. Sci. U.S.A. 110, 15561-15566
26. 2 state Angew. Chem., Int. Ed. 51, 9935-9940
27. 4Ca conformation and the H-bond network arrangement in Photosystem II Biochim. Biophys. Acta 1837, 159-166
28. 3 state Angew. Chem., Int. Ed. 52, 11744-11749
29. Glöckner, C., Kern, J., Broser, M., Zouni, A., Yachandra, V. K., and Yano, J. (2013) Structural changes of the oxygen-evolving complex in Photosystem II during the catalytic cycle J. Biol. Chem. 288, 22607-22620
30. McEvoy, J. P. and Brudvig, G. W. (2006) Water-splitting chemistry of Photosystem II Chem. Rev. 106, 4455-4483
31. Dau, H. and Haumann, M. (2007) Eight steps preceding O-O bond formation in oxygenic photosynthesis-A basis reaction cycle of the Photosystem II manganese complex Biochim. Biophys. Acta 1767, 472-483
32. Dau, H. and Haumann, M. (2008) The manganese complex of Photosystem II in its reaction cycle-basic framework and possible realization at the atomic level Coord. Chem. Rev. 252, 273-295
33. Sproviero, E. M., Gascón, J. A., McEvoy, J. P., Brudvig, G. W., and Batista, V. S. (2008) Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in Photosystem II J. Am. Chem. Soc. 130, 3428-3442
34. Dau, H., Limberg, C., Reier, T., Risch, M., Roggan, S., and Strasser, P. (2010) The mechanism of water oxidation: from electrolysis via homogeneous to biological catalysis ChemCatChem 2, 724-761
35. Klauss, A., Haumann, M., and Dau, H. (2012) Alternating electron and proton transfer steps in photosynthetic water oxidation Proc. Natl. Acad. Sci. U.S.A. 109, 16035-16040
36. McEvoy, J. P. and Brudvig, G. W. (2004) Structure-based mechanism of photosynthetic water oxidation Phys. Chem. Chem. Phys. 6, 4754-4763
37. Ishikita, H. and Knapp, E.-W. (2006) Function of redox-active tyrosine in Photosystem II Biophys. J. 90, 3886-3896
38. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center Science 303, 1831-1838
39. Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of Photosystem II Nature 438, 1040-1044
40. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Cyanobacterial Photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels, and chloride Nature Struct. Mol. Biol. 16, 334-342
41. Barber, J., Ferreira, K. N., Maghlaoui, K., and Iwata, S. (2004) Structural model of the oxygen-evolving centre of Photosystem II with mechanistic implications Phys. Chem. Chem. Phys. 6, 4737-4742
42. De Las Rivas, J. and Barber, J. (2004) Analysis of the structure of the PsbO protein and its implications Photosynth. Res. 81, 329-343
43. Bondar, A.-N. and Dau, H. (2012) Exptended protein/water H-bond networks in photosynthetic water oxidation Biochim. Biophys. Acta 1817, 1177-1190
44. Linke, K. and Ho, F. M. (2013) Water in Photosystem II: structural, functional, and mechanistic considerations Biochim. Biophys. Acta 1837, 14-32
45. Ishikita, H., Saenger, W., Loll, B., Biesiadka, J., and Knapp, E.-W. (2006) Energetics of a possible proton exit pathway for water oxidation in Photosystem II Biochemistry 45, 2063-2071
46. 4 cluster in Photosystem II based on solvent accessibility simulation, with implications for substrate water access Biochim. Biophys. Acta 1777, 140-153
47. Murray, J. W. and Barber, J. (2007) Structural characteristics of channels and pathways in Photosystem II including the identification of an oxygen channel J. Struct. Biol. 159, 228-237
48. 4Ca cluster in Photosystem II: channels calculation, noble gas derivatization, and cocrystallization with DMSO Structure 17, 1223-1234
49. Vassiliev, S., Comte, P., Mahboob, A., and Bruce, D. (2010) Tracking the flow of water through Photosystem II using molecular dynamics and streamline tracing Biochemistry 49, 1873-1881
50. Vassiliev, S., Zaraiskaya, T., and Bruce, D. (2012) Exploring the energetics of water permeation in photosystem II by multiple steered molecular dynamics simulations Biochim. Biophys. Acta 1817, 1671-1678
51. Vassiliev, S., Zaraiskaya, T., and Bruce, D. (2013) Molecular dynamics simulations reveal highly permeable oxygen exit channels shared with water uptake channels in photosystem II Biochim. Biophys. Acta 1827, 1148-1155
52. Ogata, K., Yuki, T., Hatakeyama, M., Uchida, W., and Nakamura, S. (2013) All-atom molecular dynamics simulation of Photosystem II embedded in thylakoid membranes J. Am. Chem. Soc. 135, 15670-15673
53. 5 cluster of Photosystem II: implications for the identification of oxygen channels within the photosystem Biochemistry 51, 6371-6377
54. Frankel, L. K., Sallans, L., Bellamy, H., Goettert, J. S., Limbach, P. A., and Bricker, T. M. (2013) Radiolytic mapping of solvent-contact surfaces in Photosystem II of higher plants J. Biol. Chem. 288, 23565-23572
55. Ho, F. M. (2008) Uncovering channels in photosystem II by computer modeling: current progress, future prospects, and lessons from analogous systems Photosyn. Res. 98, 503-522
56. Ho, F. M. (2012) Substrate and Proton Channels in Photosystem II, in Molecular Solar Fuels (Wydrzynski, T. and Hillier, W., Eds.) pp 208-248, Royal Society of Chemistry, Cambridge, UK.
57. Ho, F. M. (2012) Structural and mechanistic investigations of photosystem II through computational methods Biochim. Biophys. Acta 1817, 106-120
58. + Biochemistry 37, 14450-14456
59. Clausen, J., Debus, R. J., and Junge, W. (2004) Time-resolved oxygen production by PSII: chasing chemical intermediates Biochim. Biophys. Acta 1655, 184-194
60. 4Ca cluster of Photosystem II involving D1-Glu65, D2-Glu312, and D1-Glu329 Biochemistry 49, 6655-6669
61. 2 from Photosystem II Biochemistry 51, 1079-1091
62. Zscherp, C. and Barth, A. (2001) Reaction-induced infrared difference spectroscopy for the study of protein reaction mechanisms Biochemistry 40, 1875-1883
63. Barth, A. and Zscherp, C. (2002) What vibrations tell us about proteins Q. Rev. Biophys. 35, 369-430
64. Rich, P. R. and Iwaki, M. (2005) Infrared Protein Spectroscopy as a Tool to Study Protonation Reactions Within Proteins, in Biopysical and Structural Aspects of Bioenergetics (Wikström, M., Ed.) pp 314-333, Royal Society of Chemistry, Cambridge, U.K.
65. Barth, A. (2007) Infrared spectroscopy of proteins Biochim. Biophys. Acta 1767, 1073-1101
66. Berthomieu, C. and Hienerwadel, R. (2009) Fourier transform infrared (FTIR) spectroscopy Photosynth. Res. 101, 157-170
67. Noguchi, T. (2007) Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution Photosynth. Res. 91, 59-69
68. Noguchi, T. (2008) Fourier transform infrared analysis of the photosynthetic oxygen-evolving center Coord. Chem. Rev. 251, 336-346
69. Chu, H.-A. (2013) Fourier transform infrared difference spectroscopy for studying the molecular mechanism of photosynthetic water oxidation Frontiers Plant Sci. 4, 146-146
70. Noguchi, T. (2013) Monitoring the reactions of photosynthetic water oxidation using infrared spectroscopy Biomed. Spectrosc. Imaging 2, 115-128
71. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin Biochim. Biophys. Acta 1460, 177-191
72. Kandori, H. and Shichida, Y. (2000) Direct observation of the bridged water stretching vibrations inside a protein J. Am. Chem. Soc. 122, 11745-11746
73. Shibata, M. and Kandori, H. (2005) FTIR studies of internal water molecules in the Schiff base region of bacteriorhodopsin Biochemistry 44, 7406-7413
74. Garczarek, F., Brown, L. S., Lanyi, J. K., and Gerwert, K. (2005) Proton binding within a membrane protein by a protonated water cluster Proc. Natl. Acad. Sci. U.S.A. 102, 3633-3638
75. Garczarek, F. and Gerwert, K. (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy Nature 439, 109-112
76. Freier, E., Wolf, S., and Gerwert, K. (2011) Proton transfer via a transient linear water-molecule chain in a membrane protein Proc. Natl. Acad. Sci. U.S.A. 108, 11435-11439
77. Furutani, Y. and Kandori, H. (2014) Hydrogen-bonding changes of internal water molecules upon the actions of microbial rhodopsins studied by FTIR spectroscopy Biochim. Biophys. Acta 1837, 598-605
78. Breton, J. and Nabedryk, E. (1998) Proton uptake upon quinone reduction in bacterial reaction centers: IR signature and possible participation of a highly polarizable hydrogen bond network Photosynth. Res. 55, 301-307
79. Nabedryk, E. and Breton, J. (2008) Coupling of electron transfer to proton uptake at the QB site of the bacterial reaction center: a perspective from FTIR difference spectroscopy Biochim. Biophys. Acta 1777, 1229-1248
80. Iwata, T., Paddock, M. L., Okamura, M. Y., and Kandori, H. (2009) Identification of FTIR bands due to internal water molecules around the quinone binding sites in the reaction center from Rhodobacter sphaeroides Biochemistry 48, 1220-1229
81. Maréchal, A. and Rich, P. R. (2011) Water molecule reorganization in cytochrome c oxidase revealed by FTIR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 108, 8634-8638
82. Noguchi, T. and Sugiura, M. (2000) Structure of an active water molecule in the water-oxidizing complex of Photosystem II as studied by FTIR spectroscopy Biochemistry 39, 10943-10949
83. Noguchi, T. and Sugiura, M. (2002) FTIR detection of water reactions during the flash-induced S-state cycle of the photosynthetic water-oxidizing complex Biochemistry 41, 15706-15712
84. Noguchi, T. (2007) FTIR Detection of water reactions in the oxygen-evolving center of Photosystem II Philos. Trans. R. Soc., B 363, 1189-1195
85. Suzuki, H., Sugiura, M., and Noguchi, T. (2008) Monitoring water reactions during the S-state cycle of the photosynthetic water-oxidizing center: detection of the DOD bending vibrations by means of Fourier transform infrared spectroscopy Biochemistry 47, 11024-11030
86. Shimada, Y., Suzuki, H., Tsuchiya, T., Tomo, T., Noguchi, T., and Mimuro, M. (2009) Effect of a single-amino acid substitution of the 43 kDa chlorophyll protein on the oxygen-evolving reaction of the Cyanobacterium Synechocystis sp. PCC 6803: analysis of the Glu354Gln mutation Biochemistry 48, 6095-6103
87. Hou, L.-H., Wu, C.-M., Huang, H.-H., and Chu, H.-A. (2011) Effects of ammonia on the structure of the oxygen-evolving complex in Photosystem II as revealed by light-induced FTIR difference spectroscopy Biochemistry 50, 9248-9254
88. 5 cluster in Photosystem II Biochemistry 52, 8452-8464
89. Noguchi, T., Suzuki, H., Tsuno, M., Sugiura, M., and Kato, C. (2012) Time-resolved infrared detection of the proton and protein dynamics during photosynthetic oxygen evolution Biochemistry 51, 3205-3214
90. Polander, B. C. and Barry, B. A. (2013) Detection of an intermediary, protonated water cluster in photosynthetic oxygen evolution Proc. Natl. Acad. Sci. U.S.A. 110, 10634-10639
91. Chu, H.-A., Nguyen, A. P., and Debus, R. J. (1994) Site-directed Photosystem II mutants with perturbed oxygen evolving properties: 1. Instability or inefficient assembly of the manganese cluster in vivo Biochemistry 33, 6137-6149
92. Debus, R. J., Campbell, K. A., Gregor, W., Li, Z.-L., Burnap, R. L., and Britt, R. D. (2001) Does histidine 332 of the D1 polypeptide ligate the manganese cluster in Photosystem II? An electron spin echo envelope modulation study Biochemistry 40, 3690-3699
93. 3 transitions in Photosystem II Biochemistry 46, 3151-3160
94. Strickler, M. A., Walker, L. M., Hillier, W., and Debus, R. J. (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
95. Tang, X.-S. and Diner, B. A. (1994) Biochemical and spectroscopic characterization of a new oxygen-evolving Photosystem II core complex from the Cyanobacterium Synechocystis sp. PCC 6803 Biochemistry 33, 4594-4603
96. 2+ exchange in the Photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus J. Biol. Chem. 279, 22809-22819
97. 550 content of cyanobacterial Photosystem II with the EPR properties of the oxygen-evolving complex Photosynth. Res. 72, 175-189
98. Yamanari, T., Kimura, Y., Mizusawa, N., Ishii, A., and Ono, T.-A. (2004) Mid- to low-frequency Fourier transform infrared spectra of S-state cycle for photosynthetic water oxidation in Synechocystis sp. PCC 6803 Biochemistry 43, 7479-7490
99. 3 transitions in Photosystem II Biochemistry 44, 1367-1374
100. 3 transitions in Photosystem II Biochemistry 45, 8801-8811
101. Noguchi, T. and Sugiura, M. (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
102. Hays, A.-M. A., Vassiliev, I. R., Golbeck, J. H., and Debus, R. J. (1998) Role of D1-His190 in proton-coupled electron transfer reactions in Photosystem II: a chemical complementation study Biochemistry 37, 11352-11365
103. 13C-isotope labeling in S2/S1 FTIR difference spectrum of oxygen-evolving complex Biochemistry 42, 13170-13177
104. Noguchi, T., Sugiura, M., and Inoue, Y. (1999) FTIR Studies on the Amino-Acid Ligands of the Photosynthetic Oxygen-Evolving Mn-Cluster, in Fourier Transform Spectroscopy: Twelfth International Conference (Itoh, K. and Tasumi, M., Eds.) pp 459-460, Waseda University Press, Tokyo, Japan.
105. 13C isotope labeling Biochemistry 42, 6035-6042
106. Service, R. J., Yano, J., McConnell, I., Hwang, H. J., Niks, D., Hille, R., Wydrzynski, T., Burnap, R. L., Hillier, W., and Debus, R. J. (2011) Participation of glutamate-354 of the CP43 polypeptide in the ligation of manganese and the binding of substrate water in Photosystem II Biochemistry 50, 63-81
107. Pokhrel, R., Service, R. J., Debus, R. J., and Brudvig, G. W. (2013) Mutation of lysine 317 in the D2 subunit of Photosystem II alters chloride binding and proton transport Biochemistry 52, 4758-4773
108. Tommos, C. and Babcock, G. T. (2000) Proton and hydrogen currents in photosynthetic water oxidation Biochim. Biophys. Acta 1458, 199-219
109. Wraight, C. A. (2006) Chance and design-proton transfer in water, channels and bioenergetic proteins Biochim. Biophys. Acta 1757, 886-912
110. Silverman, D. N. and McKenna, R. (2007) Solvent-mediated proton transfer in catalysis by carbonic anhydrase Acc. Chem. Res. 40, 669-675
111. Mikulski, R. L. and Silverman, D. N. (2010) Proton transfer in catalysis and the role of proton shuttles in carbonic anhydrase Biochim. Biophys. Acta 1804, 422-426
112. Okamura, M. Y., Paddock, M. L., Graige, M. S., and Feher, G. (2000) Proton and electron transfer in bacterial reaction centers Biochim. Biophys. Acta 1458, 148-163
113. Paddock, M. L., Feher, G., and Okamura, M. Y. (2003) Proton transfer pathways and mechanism in bacterial reaction centers FEBS Lett. 555, 45-50
114. Wraight, C. A. (2005) Intraprotein Proton Transfer-Concepts and Realities from the Bacterial Photosynthetic Reaction Center, in Biophysical and Structural Aspects of Bioenergetics (Wikström, M., Ed.) pp 273-313, RSC Publishing, Cambridge, UK.
115. Lee, J. L., Reimann, J., Huang, Y., and Ädelroth, P. (2012) Functional proton transfer pathways in the heme-copper oxidase superfamily Biochim. Biophys. Acta 1817, 537-544
116. 3 cytochrome c oxidase from Thermus thermophilus Biochim. Biophys. Acta 1817, 650-657
117. Rich, P. R. and Maréchal, A. (2013) Functions of the hydrophilic channels in protonmotive cytochrome c oxidase J. R. Soc. Interface 10.1098/rsif.2013.0183
118. 5 cluster of Photosystem II probed with FTIR difference spectroscopy Biochemistry 53, 1001-1017
119. Suzuki, H., Yu, J., Kobayashi, T., Nakanishi, H., Nixon, P. J., and Noguchi, T. (2013) Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of Photosystem II as revealed by fourier transform infrared analysis Biochemistry 52, 4748-4757
120. Noguchi, T., Inoue, Y., and Tang, X.-S. (1999) Structure of a histidine ligand in the photosynthetic oxygen-evolving complex as studied by light-induced fourier transform infrared spectroscopy Biochemistry 38, 10187-10195
121. B Biochemistry 46, 6468-6476
122. 2-evolving complexes isolated from Synechococcus FEBS Lett. 176, 83-87
123. Saygin, Ö. and Witt, H. T. (1985) 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, 224-226
124. Rappaport, F., Blanchard-Desce, M., and Lavergne, J. (1994) Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex Biochim. Biophys. Acta 1184, 178-192
125. Kretschmann, H., Schlodder, E., and Witt, H. T. (1996) 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, 1-8
126. Mulkidjanian, A., Cherepanov, D., Haumann, M., and Junge, W. (1996) Photosystem II of green plants: topology of core pigments and redox cofactors as inferred from electrochromic difference spectra Biochemistry 35, 3093-3107
127. Ahlbrink, R., Haumann, M., Cherepanov, D., Bögershausen, O., Mulkidjanian, A., and Junge, W. (1998) Function of tyrosine-Z in water oxidation by Photosystem II: electrostatical promotor instead of hydrogen abstractor Biochemistry 37, 1131-1142
128. Rappaport, F. and Lavergne, J. (1991) Proton release during successive oxidation steps of the photosynthetic water oxidation process: stoichiometries and pH dependence Biochemistry 30, 10004-10012
129. 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 J. Biol. Chem. 274, 30387-30392
130. 2-evolving complex Biochim. Biophys. Acta 766, 403-415
131. +) nanosecond reduction kinetics in single flashes as a function of pH Biochim. Biophys. Acta 974, 36-43
132. + reduction in oxygen-evolving Photosystem II Biochemistry 41, 5015-5023