Evidence that the C-Terminus of the D1 Polypeptide of Photosystem II Is Ligated to the Manganese Ion that Undergoes Oxidation during the S1 to S2 Transition: An Isotope-Edited FTIR Study

Biochemistry

Volumn 43, Issue 11, 2004, Pages 3152-3166

  Chu, Hsiu An ^a,b,d   Hillier, Warwick ^b,c   Debus, Richard J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; ISOTOPES; NATURAL FREQUENCIES; OXIDATION; POLYPEPTIDES;

PEPTIDES; PHOTOSYSTEMS;

BIOCHEMISTRY;

ALANINE; CARBON 13; CARBONYL DERIVATIVE; MANGANESE; POLYPEPTIDE; TYROSINE;

ARTICLE; AUTOTROPHY; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CYANOBACTERIUM; INFRARED SPECTROSCOPY; ISOTOPE LABELING; NONHUMAN; OXIDATION; PHOTOCHEMISTRY; PHOTOSYSTEM II; PRIORITY JOURNAL; SYNECHOCYSTIS;

ALANINE; CARBON; CARBON ISOTOPES; CARBOXYLIC ACIDS; CATIONS, DIVALENT; CYANOBACTERIA; GLYCINE; ISOTOPE LABELING; LIGANDS; MANGANESE; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PEPTIDE FRAGMENTS; PHOTOLYSIS; PHOTOSYSTEM II PROTEIN COMPLEX; SERINE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 1542638640     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035915f     Document Type: Article

References (148)

1. Britt, R. D. (1996) Oxygen Evolution in Oxygenic Photosynthesis: The Light Reactions (Ort, D. R., and Yocum, C. F., Eds.) pp 137-164, Kluwer Academic Publishers. Dordrecht, The Netherlands.
2. Yachandra, V. K., Sauer, K., and Klein, M. P. (1996) Manganese Cluster in Photosynthesis: Where Plants Oxidize Water to Dioxygen. Chem. Rev. 96, 2927-2950.
3. Penner-Hahn, J. E. (1998) Structural Characterization of the Mn Site in the Photosynthetic Oxygen-Evolving Complex. Struct. Bonding 90, 1-36.
4. Debus, R. J. (2000) The Polypeptides of Photosystem II and Their Influence on Mangano-Tyrosyl Based Oxygen Evolution in Metal Ions in Biological Systems, Vol. 37, Manganese and Its Role in Biological Processes (Sigel, A., and Sigel, H., Eds.) pp 657-711, Marcel Dekker, New York.
5. Tommos, C., and Babcock, G. T. (2000) Proton and Hydrogen Currents in Photosynthetic Water Oxidation. Biochim. Biophys. Acta 1458, 199-219.
6. Pecoraro, V. L., and Hsieh, W.-Y. (2000) The Use of Model Complexes to Elucidate the Structure and Function of Manganese Redox Enzymes in Metal Ions in Biological Systems, Vol. 37, Manganese and Its Role in Biological Processes (Sigel, A., and Sigel, H., Eds.) pp 429-504, Marcel Dekker, Inc., New York.
7. Renger, G. (2001) Photosynthetic Water Oxidation to Molecular Oxygen: Apparatus and Mechanism. Biochim. Biophys. Acta 1503, 210-228.
8. Diner, B. A., and Rappaport, F. (2002) Structure, Dynamics, and Energetics of the Primary Photochemistry of Photosystem II of Oxygenic Photosynthesis. Annu. Rev. Plant Biol. 53, 551-580.
9. Goussias, C., Boussac, A., and Rutherford, A. W. (2002) Photosystem II and Photosynthetic Oxidation of Water: An Overview. Philos. Trans. R. Soc. London, Ser. B 357, 1369-1381.
10. Cinco, R. M., Holman, K. L., Robblee, J. H., Yano, J., Pizarro, S. A., Bellacchio, E., Sauer, K., and Yachandra, V. K. (2002) Calcium EXAFS Establishes the Mn-Ca Cluster in the Oxygen-Evolving Complex of Photosystem II. Biochemistry 41, 12928-12933.
11. 2-state Multiline Signal ESEEM Study. J. Am. Chem. Soc. 124, 10921-10933.
12. Faller, P., Debus, R. J., Brettel, K., Sugiura, M., Rutherford, A. W., and Boussac, A. (2001) Rapid Formation of the Stable Tyrosyl Radical in Photosystem II. Proc. Natl. Acad. Sci. U.S.A. 98, 14368-14373.
13. Ananyev, G. A., Sakiyan, I., Diner, B. A., and Dismukes, G. C. (2002) A Functional Role for Tyrosine-D in Assembly of the Inorganic Core of the Water Oxidase Complex of Photosystem II and the Kinetics of Water Oxidation. Biochemistry 41, 974-980.
14. Robblee, J. H., Cinco, R. M., and Yachandra, V. K. (2001) X-ray Spectroscopy-Based Structure of the Mn Cluster and Mechanism of Photosynthetic Oxygen Evolution. Biochim. Biophys. Acta 1503, 7-23.
15. Dau, H., Iuzzolino, L., and Dittmer, J. (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.
16. Yachandra, V. K. (2002) Structure of the Manganese Complex in Photosystem II: Insights from X-ray Spectroscopy. Philos. Trans. R. Soc. London, Ser. B 357, 1347-1358.
17. 2 State Multiline EPR Signals. Inorg. Chem. 35, 3307-3319.
18. Carrell, T. G., Tyryshkin, A. M., and Dismukes, G. C. (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.
19. 3 Transition: Implications for the Mechanism of Photosynthetic Water Oxidation. J. Am. Chem. Soc. 123, 7804-7820.
20. 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 Å Resolution. Nature 409, 739-743.
21. Fromme, P., Kern, J., Loll, B., Biesiadka, J., Saenger, W., Witt, H. T., Krauss, N., and Zouni, A. (2002) Functional Implication on the Mechanism of the Function of Photosystem II Including Water Oxidation base on the Structure of Photosystem II. Philos. Trans. R. Soc. London, Ser. B 357, 1337-1345.
22. Kamiya, N., and Shen, J.-R. (2003) Crystal Structure of Oxygen-Evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Å Resolution. Proc. Natl. Acad. Sci. U.S.A. 100, 98-103.
23. 2-state Multiline EPR Signal of Photosystem II: Implications on the Structure of the Tetranuclear Mn Cluster. J. Am. Chem. Soc. 122, 10926-10942.
24. Peloquin, J. M., and Britt, R. D. (2001) EPR/ENDOR Characterization of the Physical and Electronic Structure of the OEC Mn Cluster. Biochim. Biophys. Acta 1503, 96-111.
25. Diner, B. A. (2001) Amino Acid Residues Involved in the Coordination and Assembly of the Manganese Cluster of Photosystem II: Proton-Coupled Electron Transport of the Redox-Active Tyrosines and Its Relationship to Water Oxidation. Biochim. Biophys. Acta 1503, 147-163.
26. z and the Manganese Cluster in the Water Oxidizing Complex of Photosystem II. Biochim. Biophys. Acta 1503, 164-186.
27. 2 Evolving Site as Analyzed by Site-Directed Mutagenesis in The Water/Plastoquinone Oxido-Reductase of Photosynthesis (Wydrzynski, T., and Satoh, Ki., Eds.) Kluwer Academic Publishers, Dordrecht, The Netherlands, in press.
28. 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.
29. Debus, R. J., Aznar, C., Campbell, K. A., Gregor, W., Diner, B. A., and Britt, R. D. (2003) Does Aspartate 170 of the D1 Polypeptide Ligate the Manganese Cluster in Photosystem II? An EPR and ESEEM Study. Biochemistry 42, 10600-10608.
30. Chu, H.-A., Debus, R. J., and Babcock, G. T. (2001) D1-Asp170 is Structurally Coupled to the Oxygen Evolving Complex in Photosystem II as Revealed by Light-Induced Fourier Transform Infrared Difference Spectroscopy. Biochemistry 40, 2312-2316.
31. Mäntele, W. (1996) Infrared and Fourier Transform Infrared Spectroscopy in Biophysical Techniques in Photosynthesis (Amesz, J., and Hoff, A. J., Eds.) pp 137-160, Kluwer Academic Publishers, Dordrecht, The Netherlands.
32. Vogel, R., and Siebert, F. (2000) Vibrational Spectroscopy as a Tool for Probing Protein Function. Curr. Opin. Chem. Biol. 4, 518-523.
33. Zscherp, C., and Barth, A. (2001) Reaction-Induced Infrared Difference Spectroscopy for the Study of Protein Reaction Mechanisms. Biochemistry 40, 1875-1883.
34. Barth, A., and Zscherp, C. (2002) What Vibrations Tell Us About Proteins. Q. Rev. Biophys. 35, 369-430.
35. Chu, H.-A., Hillier, W., Law, N. A., and Babcock, G. T. (2001) Vibrational Spectroscopy of the Oxygen-Evolving Complex and of Manganese Model Compounds. Biochim. Biophys. Acta 1503, 69-82.
36. Noguchi, T., and Berthomieu, C. (2004) Molecular Analysis by Vibrational Spectroscopy in Photosystem II: The Water/Plastoquinone Oxido-Reductase of Photosynthesis (Wydrzynski, T., and Satoh, Ki., Eds.) Kluwer Academic Publishers, Dordrecht, The Netherlands, in press.
37. 2+ in the Photosynthetic Oxygen-Evolving Center by Means of Fourier Transform Infrared Spectroscopy. Biochim. Biophys. Acta 1228, 189-200.
38. 1 FTIR Spectrum in Oxygen-Evolving Complex of Photosystem II. Biochemistry 40, 14061-14068.
39. Noguchi, T., Ono, T.-A., and Inoue, Y. (1995) A Carboxylate Ligand Interacting with Water in the Oxygen-Evolving Center of Photosystem II as Revealed by Fourier Transform Infrared Spectroscopy. Biochim. Biophys. Acta 1232, 59-66.
40. 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.
41. 13C isotope Labeling. Biochemistry 42, 6035-6042.
42. 1 FTIR Difference Spectrum of Oxygen-Evolving Complex. Biochemistry 42, 13170-13177.
43. Noguchi, T., Inoue, Y., and Tang, X. S. (1997) Structural Coupling between the Oxygen-Evolving Mn Cluster and a Tyrosine Residue in Photosystem II as Revealed by Fourier Transform Infrared Spectroscopy. Biochemistry 36, 14705-14711.
44. 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.
45. Nixon, P. J., Trost, J. T., and Diner, B. A. (1992) 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 31, 10859-10871.
46. Kashino, Y., Lauber, W. M., Carroll, J. A., Wang, Q. J., Whitmarsh, J., Satoh, Ka., and Pakrasi, H. B. (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.
47. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okamura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M., and Tabata, S. (1996) Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC 6803. II. Sequence Determination of the Entire Genome and Assignment of Potential Protein-Coding Regions. DNA Res. 3, 109-136, Suppl. 185-209.
48. Ikeuchi, M., and Tabata, S. (2001) Synechocystis sp. PCC 6803 - a Useful Tool in the Study of the Genetics of Cyanobacteria. Photosynth. Res. 70, 73-83.
49. Chu, H.-A., Babcock, G. T., and Debus, R. J. (2001) Possible Ligation of the Mn cluster in Photosystem II by the Carboxyl-Terminus of the D1 Polypeptide: An FTIR Study in PS2001 Proceedings: 12th International Congress on Photosynthesis, paper S13-P026, pp 1-4, CSIRO Publishing, Melbourne, Australia (published on the web: www.publish.csiro.au/PS2001).
50. Williams, J. G. K. (1988) Construction of Specific Mutations in Photosystem II Photosynthetic Reaction Center by Genetic Engineering Methods in Synechocystis 6803. Methods Enzymol. 167, 766-778.
51. Chu, H.-A., Nguyen, A. P., and Debus, R. J. (1994) Site-Directed Photosystem II Mutants with Perturbed Oxygen Evolving Properties. 2. Increased Binding or Photooxidation of Manganese in the Absence of the Extrinsic 33-kDa Polypeptide In Vivo. Biochemistry 33, 6150-6157.
52. Chu, H.-A., Nguyen, A. P., and Debus, R. J. (1995) Amino Acid Residues that Influence the Binding of Manganese or Calcium to Photosystem II. 2. The Carboxy-terminal Domain of the D1 Polypeptide. Biochemistry 34, 5859-5882.
53. Debus, R. J., Nguyen, A. P., and Conway, A. B. (1990) Identification of Ligands to Manganese and Calcium in Photosystem II by Site-Directed Mutagenesis in Current Research in Photosynthesis (Baltscheffsky, M., Ed.) Vol. I, pp 829-832, Kluwer Academic Publishers, Dordrecht, The Netherlands.
54. 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.
55. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y. (1979) Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. J. Gen. Microbiol. 111, 1-61.
56. A Binding Pocket of PSII Reaction Centers from Spinach and Synechocystis. Biochemistry 38, 2057-2067.
57. Hays, A.-M. A., Vassiliev, I. R., Golbeck, J. H., and Debus, R. J. (1998) Role of D1-His 190 in Proton-Coupled Electron-Transfer Reactions in Photosystem II: A Chemical Complementation Study. Biochemistry 37, 11352-11365.
58. Peiffer, W. E., Ingle, R. T., and Ferguson-Miller, S. (1990) Structurally Unique Plant Cytochrome c Oxidase Isolated from Wheat Germ, a Rich Source of Plant Mitochondrial Enzyme. Biochemistry 29, 8696-8701.
59. Das Neves, H. J. C., and Vasconcelos, A. M. P. (1987) Capillary Gas Chromatography of Amino Acids, Including Asparagine and Glutamine: Sensitive Gas Chromatographic-Mass Spectrometric and Selected Ion Monitoring Gas Chromatographic-Mass Spectrometric Detection of the N,O(S)-tert-Butyldimethylsilyl Derivatives, J. Chromatogr. 392, 249-258.
60. Schwender, J., and Ohlrogge, J. B. (2002) Probing In Vivo Metabolism by Stable Isotope Labeling of Storage Lipids and Proteins in Developing Brassica napus Embryos. Plant Physiol. 130, 347-361.
61. Chu, H.-A., Gardner, M. T., Hillier, W., and Babcock, G. T. (2000) Low-Frequency Fourier Transform Infrared Spectroscopy of the Oxygen-Evolving Complexes in Photosystem II. Photosyn. Res. 66, 57-63.
62. Hillier, W., and Babcock, G. T. (2001) S-State Dependent FTIR Difference Spectra for the Photosystem II Oxygen Evolving Complex. Biochemistry 40, 1503-1509.
63. 2 State. Photosynth. Res. 63, 47-57.
64. Noguchi, T., and Sugiura, M. (2000) Structure of an Active Water Molecule in the Water-Oxidizing Complex of Photosystem II as Studied by FTIR Sectroscopy. Biochemistry 39, 10943-10949.
65. Hatano-Iwasaki, A., Minagawa, J., Inoue, Y., and Takahashi, Y. (2001) Two Functionally Distinct Manganese Clusters formed by Introducing a Mutation in the Carboxyl Terminus of a Photosystem II Reaction Center Polypeptide, D1, of the Green Alga Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1504, 299-310.
66. Chu, H.-A., Gardner, M. T., O'Brien, J. P., and Babcock, G. T. (1999) Low-frequency Fourier Transform Infrared Spectroscopy of the Oxygen-Evolving and Quinone Acceptor Complexes in Photosystem II. Biochemistry 38, 4533-4541.
67. Susi, H., and Byler, D. M. (1980) Vibrational Analysis of L-Alanine and Deuterated Analogs. J. Mol. Struct. 63, 1-11.
68. Diem, M., Polavarapu, P. L., Oboodi, M., and Nafie, L. A. (1982) Vibrational Circular Dichroism in Amino Acids and Peptides. 4. Vibrational Analysis, Assignments, and Solution-Phase Raman Spectra of Deuterated Isotopomers of Alanine. J. Am. Chem. Soc. 104, 3329-3336.
69. Diem, M. (1988) Infrared Vibrational Circular Dichrosim of Alanine in the Midinfrared Region: Isotopic Effects, J. Am. Chem. Soc. 110, 6967-6970,
70. Tortonda, F. R., Pascual-Ahuir, J.-L., Silla, E., Tunon, I., and Ramirez, F. (1998) Aminoacid Zwitterions in Solution: Geometric, Energetic, and Vibrational Analysis Using Density Functional Theory-Continuum Model Calculations. J. Chem. Phys. 109, 592-603.
71. Noguchi, T., and Sugiura, M. (2001) Flash-Induced Fourier Transform Infrared Detection of the Structural Changes during the S-State Cycle of the Oxygen-Evolving Complex in Photosystem II. Biochemistry 40, 1497-1502.
72. 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.
73. 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.
74. 2 Transition in the Oxygen-Evolving Manganese Cluster in Photosystem II by Light-Induced Fourier Transform Infrared Difference Spectroscopy. Biochemistry 31, 5953-5956.
75. 2 Transition in the Oxygen-Evolving Complex of Photosystem II Studied by FT-IR Spectroscopy. Biochim. Biophys. Acta 1143, 333-336.
76. B of Photosystem II Determined by Time-Resolved Fourier Transform Infrared Spectroscopy. Biochemistry 37, 5511-5517.
77. 3 Transition of the Oxygen-Evolving Complex in Photosystem II. Biochim. Biophys. Acta 1459, 528-532.
78. 2+ Depletion and Metal Cation Substitution in the Photosynthetic Oxygen-Evolving Complex. Biochemistry 41, 5844-5853.
79. Hasegawa, K., Kimura, Y., and Ono, T.-A. (2002) Chloride Cofactor in Photosynthetic Oxygen-Evolving Complex studied by FTIR Spectroscopy. Biochemistry 41, 13839-13850.
80. 1 FTIR Spectrum in Photosynthetic Oxygen-Evolving Complex. J. Inorg. Biochem. 97, 231-239.
81. 680+ Reduction Kinetics and Redox Transition Probability of the Water Oxidizing Complex as a Function of the pH and the H/D Isotope Exchange in Spinach Thylkoids. Biochemistry 38, 6082-6092.
82. Isgandarova, S., Renger, G., and Messinger, J. (2003) Functional Differences of Photosystem II from Synechococcus elongatus and Spinach Characterized by Flash Induced Oxygen Evolution Patterns. Biochemistry 42, 8929-8938.
83. 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. Proc. Natl. Acad. Sci. U.S.A. 93, 3335-3340.
84. De Wijn, R., Schrama, T., and van Gorkom, H. J. (2001) Secondary Stabilization Reactions and Proton-Coupled Electron Transport in Photosystem II Investigated by Electroluminescence and Fluorescence Spectroscopy. Biochemistry 40, 5821-5834.
85. De Wijn, R., and van Gorkom, H. J. (2002) S-state Dependence of the Miss Probability in Photosystem II. Photosynth. Res. 72, 217-222.
86. 2 state in Photosynthetic Oxygen Evolution: A Difference FT-IR study. J. Phys. Chem. B 101, 6652-6660.
87. Steenhuis, J. J., and Barry, B. A. (1998) Difference FT-IR studies of Photoassembly in the Manganese-Containing Catalytic Site of Photosystem. J. Phys. Chem. B 102, 4-8.
88. Steenhuis, J. J., Hutchison, R. S., and Barry, B. A. (1999) Alterations in Carboxylate Ligation at the Active Site of Photosystem II. J. Biol. Chem. 274, 14609-14616.
89. Hutchison, R. S., Steenhuis, J. J., Yocum, C. F., Razeghifard, M. R., and Barry, B. A. (1999) Deprotonation of the 33-kDa, Extrinsic, Manganese-Stabilizing Subunit Accompanies Photooxidation of Manganese in Photosystem II. J. Biol. Chem. 274, 31987-31995.
90. Halverson, K. M., and Barry, B. A. (2003) Evidence for Spontaneous Structural Changes in a Dark-Adapted State of Photosystem II. Biophys. J. 85, 2581-2588.
91. Barry, B. A. (2000) FT-IR spectroscopic studies of the S state transitions. Photosynth. Res. 65, 197-198.
92. Mehrotra, R. C., and Bohra, R. (1983) Metal Carboxylates, pp 48-60, Academic Press, London, UK.
93. Nara, M., Torii, H., and Tasumi, M. (1996) Correlation between the Vibrational Frequencies of the Carboxylate Group and Types of its Coordination to a Metal Ion: An ab Initio Molecular Orbital Study. J. Phys. Chem. 100, 19812-19817.
94. Krimm, S., and Bandekar, J. (1986) Vibrational Spectroscopy and Conformation of Peptides, Polypeptides, and Proteins. Adv. Protein Chem. 38, 181-364.
95. Tadesse, L., Nazarbaghi, R., and Walters, L. (1991) Isotopically Enhanced Infrared Spectroscopy: A Novel Method for Examining Secondary Structure at Specific Sites in Conformationally Heterogeneous Peptides, J. Am. Chem. Soc. 113, 7036-7037.
96. 15N Labeling for Studying Protein-Protein Interactions Using Fourier Transform Infrared Spectroscopy. Biochemistry 31, 6279-6284.
97. Zhang, M., Fabian, H., Mantsch, H. H., and Vogel, H. J. (1994) Isotope-Edited Fourier Transform Infrared Spectroscopy Studies of Calmodulin's Interaction with Its Target Peptides. Biochemistry 33, 10883-10888.
98. Noguchi, T., and Inoue, Y. (1995) Molecular Interactions of the Redox-Active Accessory Chlorophyll on the Electron-Donor Side of Photosystem II as Studied by Fourier Transform Infrared Spectroscopy. FEBS Lett. 370, 241-244.
99. Noguchi, T., Mitsuka, T., and Inoue, Y. (1994) Fourier Transform Infrared Spectrum of the Radical Cation of β-Carotene Photoinduced in Photosystem II. FEBS Lett. 356, 179-182.
100. Berthomieu, C., Hienerwadel, R., Boussac, A., Breton, J., and Diner, B. A. (1998) Hydrogen-Bonding of Redox-Active Tyrosine Z of Photosystem II Probed by FTIR Difference Spectroscopy. Biochemistry 37, 10547-10554.
101. A in Photosystem II. FEBS Lett. 269, 363-367.
102. A Reduction in Photosystem II. Biochemistry 35, 15447-15460.
103. Z Interactions in Photosystem II. Biochemistry 36, 11762-11768.
104. A Photoreduction in Photosystem II Core Particles in Photosynthesis: Mechanisms and Effects (Garab, G., Ed.) Vol. II, pp 1121-1124, Kluwer Academic Publishers, Dordrecht, The Netherlands.
105. Faller, P., Pascal, A., and Rutherford, A. W. (2001) β-carotene redox reactions in photosystem II: Electron-transfer pathway. Biochemistry 40, 6431-6440.
106. Tracewell, C. A., Cua, A., Stewart, D. H., Bocian, D. F., and Brudvig, G. W. (2001) Characterization of Carotenoid and Chlorophyll Photooxidation in Photosystem II. Biochemistry 40, 193-203.
107. Tracewell, C. A., and Brudvig, G. W. (2003) Two Redox-Active β-Carotene Molecules in Photosystem II. Biochemistry 42, 9127-9136.
108. Noguchi, T., and Inoue, Y. (1995) Identification of Fourier Transform Infrared Signals from the Non-Heme Iron in Photosystem II. J. Biochem. 118, 9-12.
109. 13C-Labeled Bicarbonate. Biochemistry 34, 16288-16297.
110. B pocket Studied by Fourier Transform Infrared Spectroscopy. Biochemistry 40, 4044-4052.
111. Berthomieu, C., Boussac, A., Mäntele, W., Breton, J., and Nabedryk, E. (1992) Molecular Changes following Oxidoreduction of Cytochrome b559 Characterized by Fourier Transform Infrared Difference Spectroscopy and Electron Paramagnetic Resonance: Photooxidation in Photosystem II and Electrochemistry of Isolated Cytochrome b559 and Iron Protoporphyrin IX-Bisimidazole Model Compounds. Biochemistry 31, 11460-11471.
112. Hienerwadel, R., Boussac, A., Breton, J., Diner, B. A., and Berthomieu, C. (1997) Fourier Transform Infrared Difference Spectroscopy of Photosystem II Tyrosine D using Site-Directed Mutagenesis and Specific Isotope Labeling. Biochemistry 36, 14712-14723.
113. . in Photosystem II: A Comparative Biochemical and Kinetic Study. Biochemistry 37, 13882-13892.
114. . Radicals in Photosystem II. Biochim. Biophys. Acta 1366, 331-354.
115. O'Malley, P. J. (2002) Density Functional Calculations Modelling Tyrosine Oxidation in Oxygenic Photosynthetic Electron Transfer. Biochim. Biophys. Acta 1553, 212-217.
116. Diner, B. A., Tang, X.-S., Zheng, M., Dismukes, G. C., Force, D. A., Randall, D. W., and Britt, R. D. (1995) Environment and Function of the Redox Active Tyrosines of Photosystem II in Photosynthesis: From Light to Biosphere (Mathis, P., Ed.) Vol. II, pp 229-234, Kluwer Academic Publishers, Dordrecht.
117. Faller, P., Rutherford, A. W., and Debus, R. J. (2002) Tyrosine D oxidation at cryogenic temperature in photosystem II. Biochemistry 41, 12914-12920.
118. Faller, P., Goussias, C., Rutherford, A. W., and Un, S. (2003) Resolving Intermediates in Biological Proton-Coupled Electron Transfer: A Tyrosyl Radical Prior to Proton Movement. Proc. Natl. Acad. Sci. U.S.A. 100, 8732-8735.
119. Reinman, S., and Mathis, P. (1981) Influence of Temperature on Photosystem II Electron-Transfer Reactions. Biochim. Biophys. Acta 635, 249-258.
120. . Decay Kinetics in Tris-treated PSII Particles Studied by Time-Resolved EPR. Plant Cell Physiol. 38, 1007-1011.
121. Kühne, H., and Brudvig, G. W. (2002) Proton-Coupled Electron Transfer Involving Tyrosine Z in Photosystem II. J. Phys. Chem. B 106, 8189-8196.
122. Deacon, G. B., and Phillips, R. J. (1980) Relationships between the Carbon-Oxygen Stretching Frequencies of Carboxylato Complexes and the Type of Carboxylate Coordination. Coord. Chem. Rev. 33, 227-250.
123. Tackett, J. E. (1989) FT-IR Characterization of Metal Acetates in Aqueous Solution. Appl. Spectrosc. 43, 483-489.
124. Nakamoto, K. (1997) Infrared and Raman Spectra of Inorganic and Coordination Compounds, Part B: Applications in Coordination, Organometallic, and Bioinorganic Chemistry, 5th ed., pp 59-62, John Wiley & Sons, New York.
125. 2O) Solutions. 1. Spectral Parameters of Amino Acid Residue Absorption Bands. Biopolymers 30, 1243-1257.
126. Barth, A. (2000) The Infrared Absorption of Amino Acid Side Chains. Prog. Biophys. Mol. Biol. 74, 141-173.
127. Rahmelow, K., Hübner, W., and Ackermann, Th. (1998) Infrared Absorbances of Protein Side Chains. Anal. Biochem. 257, 1-11.
128. Smith, J. C., Gonzalez-Vergara, E., and Vincent, J. B. (1997) Detection of Structural Changes upon Oxidation in Multinuclear Mn-Oxo-Carboxylate Assemblies by Fourier Transform Infrared Spectroscopy: Relationship to Photosystem II. Inorg. Chim. Acta 255, 99-103.
129. Czarnecki, K., Kirmaier, C., Holten, D., and Bocian, D. F. (1999) Vibrational and Photochemical Consequences of an Asp Residue Near the Photoactive Accessory Bacteriochlorophyll in the Photosynthetic Reaction Center. J. Phys. Chem. A 103, 2235-2246.
130. Tommos, C., Hoganson, C. W., Di Valentin, M., Lydakis-Simantiris, N., Dorlet, P., Westphal, K., Chu, H.-A., McCracken, J., and Babcock, G. T. (1998) Manganese and Tyrosyl Radical Function in Photosynthetic Oxygen Evolution. Curr. Opin. Chem. Biol. 2, 244-252.
131. Tommos, C. (2002) Electron, Proton, and Hydrogen-Atom Transfers in Photosynthetic Water Oxidation. Philos. Trans. R. Soc. London, Ser. B 357, 1383-1394.
132. 2-Evolving Complexes Isolated from Synechococcus. FEBS Lett. 176, 83-87.
133. 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.
134. 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.
135. 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.
136. 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.
137. 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.
138. 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.
139. 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.
140. Rappaport, F., and Lavergne, J. (2001) Coupling of Electron and Proton Transfer in the Photosynthetic Water Oxidase. Biochim. Biophys. Acta 1503, 246-259.
141. Junge, W., Haumann, M., Ahlbrink, R., Mulkidjanian, A., and Clausen, J. (2002) Electrostatics and Proton Transfer in Photosynthetic Water Oxidation, Philos. Trans. R. Soc. London, Ser. B 357, 1407-1418.
142. 2-Evolving Complex. Biochim. Biophys, Acta 766, 403-415.
143. +) Nanosecond Reduction Kinetics in Single Flashes as a Function of pH. Biochim. Biophys. Acta 974, 36-43.
144. + Reduction in Oxygen-Evolving Photosystem. Biochemistry 41, 5015-5023.
145. Zhao, X. G., Richardson, W. H., Chen, J.-L., Li, J., Noodleman, L., Tsai, H.-L., and Hendrickson, D. N. (1997) Density Functional Calculations of Electronic Structure, Charge Distribution, and Spin Coupling in Manganese-Oxo Dimer Complexes. Inorg. Chem. 36, 1198-1217.
146. McGrady, J. E., and Stranger, R. (1997) Redox-Induced Changes in the Geometry and Electronic Structure of Di-μ-Oxo-Bridged Manganese Dimers. J. Am. Chem. Soc. 119, 8512-8522.
147. Delfs, C. D., and Stranger, R. (2001) Oxidation State Dependence of the Geometry, Electronic Structure, and Magnetic Coupling in Mixed Oxo- and Carboxylato-Bridged Manganese Dimers. Inorg. Chem. 40, 3061-3076.
148. Barone, V., Bencini, A., Gatteschi, D., and Totti, F. (2002) DFT Description of the Magnetic Properties and Electron Localization in Dinuclear Di-μ-Oxo-Bridged Manganese Complexes. Chem. Eur. J. 8, 5019-5027.