Participation of glutamate-333 of the D1 polypeptide in the ligation of the Mn4CaO5 cluster in photosystem II

Biochemistry

Volumn 52, Issue 47, 2013, Pages 8452-8464

  Service, Rachel J ^a,e   Yano, Junko ^b   Dilbeck, Preston L ^c,f   Burnap, Robert L ^c   Hillier, Warwick ^d   Debus, Richard J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c OKLAHOMA STATE UNIVERSITY   (United States)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^f WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; CYANOBACTERIUM SYNECHOCYSTIS; DIOXYGEN MOLECULES; FTIR DIFFERENCE SPECTROSCOPY; PSII CORE COMPLEX; SPECTROSCOPIC METHOD; STRETCHING REGION; STRUCTURAL MODELING;

AMINO ACIDS; ATOMS; CARBOXYLATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN BONDS; MANGANESE; MOLECULES; OXYGEN; POLYPEPTIDES; SPECTROSCOPIC ANALYSIS;

MANGANESE COMPOUNDS;

ALGAL PROTEIN; AMIDE; BACTERIAL PROTEIN; CALCIUM; CARBONYL DERIVATIVE; CARBOXYLIC ACID; D1 POLYPEPTIDE; GLUTAMIC ACID; MANGANESE; OXYGEN; POLYPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; CATALYSIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; HYDROGEN BOND; INFRARED SPECTROSCOPY; KINETICS; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTATION; NONHUMAN; PHOTOSYSTEM II; POLAROGRAPHY; PRIORITY JOURNAL; PROTON TRANSPORT; SYNECHOCYSTIS; WILD TYPE; X RAY ABSORPTION SPECTROSCOPY;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BIOCATALYSIS; CALCIUM; CARBOXYPEPTIDASES; ELECTRON SPIN RESONANCE SPECTROSCOPY; GLUTAMIC ACID; HYDROGEN BONDING; KINETICS; MANGANESE; MODELS, MOLECULAR; MUTANT PROTEINS; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PROPROTEIN CONVERTASES; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SYNECHOCYSTIS; X-RAY ABSORPTION SPECTROSCOPY;

EID: 84888622333     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401339f     Document Type: Article

References (88)

1. 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
2. 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
3. Barber, J. (2012) Photosystem II: The Water-Splitting Enzyme of Photosynthesis, Cold Spring Harbor Symp Quant. Biol. 77, 295-307
4. 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
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. 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: Biol. 104, 9-18
11. 2-Evolving Complex of Photosystem II Biochemistry 50, 6308-6311
12. Ames, W., Pantazis, D. A., Krewald, V., Cox, N., Messinger, J., Lubitz, W., and Neese, F. (2011) Theoretical Evaluation of Structural Models of the S2 State in the Oxygen Evolving Complex of Photosystem II: Protonation States and Magnetic Interactions J. Am. Chem. Soc. 133, 19743-19757
13. 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
14. 4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence J. Photochem. Photobiol., B: Biol. 104, 100-110
15. 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
16. 3 states of oxygen-evolving complex of photosystem II: full geometry optimizations by B3LYP hybrid density functional Dalton Trans. 41, 13727-13740
17. 2 Formation in Photosystem II Acc. Chem. Res. 42, 1871-1880
18. 4 cluster of PSII refined to 1.9 Å resolution Chem. Phys. Lett. 511, 138-145
19. 4 transitions in photosystem II Phys. Chem. Chem. Phys. 14, 4849-4856
20. 17O Electron-Electron Double Resonance-Detected NMR Spectroscopy J. Am. Chem. Soc. 134, 16619-16634
21. 2 release Biochim. Biophys. Acta 1827, 1003-1019
22. 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
23. 2 State Angew. Chem., Int. Ed. 51, 9935-9940
24. 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
25. 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
26. 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
27. McEvoy, J. P. and Brudvig, G. W. (2006) Water-Splitting Chemistry of Photosystem II Chem. Rev. 106, 4455-4483
28. 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
29. 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
30. 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
31. 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
32. Nixon, P. J. and Diner, B. A. (1994) Analysis of Water-Oxidation Mutants Constructed in the Cyanobacterium Synechocystis sp. PCC 6803 Biochem. Soc. Trans. 22, 338-343
33. 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
34. 4Ca Cluser of Photosystem II J. Biol. Chem. 282, 7209-7218
35. 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
36. 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
37. 3 Transitions in Photosystem II Biochemistry 46, 3151-3160
38. 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
39. 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
40. 2+ Exchange in the Photosystem II Oxygen-Evolving Enzyme of Thermosynechococcus elongatus J. Biol. Chem. 279, 22809-22819
41. 550 content of cyanobacterial Photosystem II with the EPR properties of the oxygen-evolving complex Photosynth. Res. 72, 175-189
42. 2O Oxidation Complex in Synechocystis sp. PCC 6803 Biochemistry 35, 874-882
43. 2O-Oxidation in Synechocystis sp. PCC 6803 Biochemistry 38, 6070-6081
44. 2 from Photosystem II Biochemistry 51, 1079-1091
45. Lavorel, J. (1976) Matrix Analysis of the Oxygen Evolving System of Photosynthesis J. Theor. Biol. 57, 171-185
46. Meunier, P. C., Burnap, R. L., and Sherman, L. A. (1996) Improved 5-step Modeling of the Photosystem II S-state Mechanism in Cyanobacteria Photosynth. Res. 47, 61-76
47. Jursinic, P. A. and Dennenberg, R. J. (1990) Oxygen Release Time in Leaf Discs and Thylakoids of Peas and Photosystem II Membrane Fragments of Spinach Biochim. Biophys. Acta 1020, 195-206
48. 4Ca Cluster J. Am. Chem. Soc. 14974-14975
49. 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
50. 3 Transitions in Photosystem II Biochemistry 44, 1367-1374
51. 3 Transitions in Photosystem II Biochemistry 45, 8801-8811
52. 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
53. 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
54. 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
55. 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
56. Noguchi, T. and Berthomieu, C. (2005) Molecular Analysis by Vibrational Spectroscopy, in Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T. and Satoh, Ki., Eds.) pp 367-387, Springer, Dordrecht, The Netherlands.
57. 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
58. Noguchi, T. (2008) Fourier Transform Infrared Analysis of the Photosynthetic Oxygen-Evolving Center Coord. Chem. Rev. 251, 336-346
59. 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
60. 4Ca Cluster of Photosystem II Involving D1-Glu65, D2-Glu312, and D1-Glu329 Biochemistry 49, 6655-6669
61. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin Biochim. Biophys. Acta 1460, 177-191
62. 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
63. 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
64. Garczarek, F. and Gerwert, K. (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy Nature 439, 109-112
65. 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
66. 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
67. 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
68. Burnap, R. L. (2004) D1 Protein Processing and Mn Cluster Assembly in Light of the Emerging Photosystem II Structure Phys. Chem. Chem. Phys. 6, 4803-4809
69. DasGupta, J., Ananyev, G. M., and Dismukes, G. C. (2008) Photoassembly of the Water-Oxidizing Complex in Photosystem II Coord. Chem. Rev. 252, 347-360
70. Becker, K., Cormann, K. U., and Nowaczyk, M. M. (2011) Assembly of the Water-Oxidizing Complex in Photosystem II J. Photochem. Photobiol., B: Biol. 104, 204-211
71. 2O-Oxidation Complex of Photosystem II Biochemistry 46, 13648-13657
72. 4Ca Cluster in the Oxygen Evolving Complex of Photosystem II by a Histidine Ligand Mutation J. Biol. Chem. 286, 9257-9267
73. 2-state Multiline EPR Signal of Photosystem II: Implications on the Structure of the Tetranuclear Mn Cluster J. Am. Chem. Soc. 122, 10926-10942
74. 55Mn-ENDOR and EPR Spectroscopy J. Am. Chem. Soc. 129, 13421-13435
75. 2 State J. Am. Chem. Soc. 133, 3635-3648 (Correction pg. 14149)
76. 2 states of the oxygen-evolving complexes of photosystem II in plants and cyanobacteria in the presence and absence of methanol Biochim. Biophys. Acta 1807, 829-840
77. Stich, T. A., Yeagle, G. J., Service, R. J., Debus, R. J., and Britt, R. D. (2011) Ligation of D1-His332 and D1-Asp170 to the Manganese Cluster of Photosystem II from Synechocystis Assessed by Multifrequency Pulse EPR Spectroscopy Biochemistry 50, 7390-7404
78. Z in Photosystem II Biochemistry 39, 470-478
79. 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
80. Kimura, Y., Mizusawa, N., Ishii, A., Nakazawa, S., and Ono, T.-A. (2005) Changes in Structural and Functional Properties of Oxygen-Evolving Complex Induced by Replacement of D1-Glutamate 189 with Glutamine in Photosystem II: Ligation of Glutamate 189 Carboxylate to the Manganese Cluster J. Biol. Chem. 280, 37895-37900
81. 2 Transition: An Isotope-Edited FTIR Study Biochemistry 43, 3152-3166
82. Mizusawa, N., Kimura, Y., Ishii, A., Yamanari, T., Nakazawa, S., Teramoto, H., and Ono, T.-A. (2004) Impact of Replacement of D1 C-terminal Alanine with Glycine on Structure and Function of Photosynthetic Oxygen-Evolving Complex J. Biol. Chem. 279, 29622-29627
83. Mizusawa, N., Yamanari, T., Kimura, Y., Ishii, A., Nakazawa, S., and Ono, T.-A. (2004) Changes in the Functional and Structural Properties of the Mn Cluster Induced by Replacing the Side Group of the C-Terminus of the D1 Protein of Photosystem II Biochemistry 43, 14644-14652
84. Kimura, Y., Mizusawa, N., Yamanari, T., Ishii, A., and Ono, T.-A. (2005) Structural Changes of D1 C-terminal α-Carboxylate during S-state Cycling of Photosynthetic Oxygen Evolution J. Biol. Chem. 280, 2078-2083
85. 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
86. Bondar, A.-N. and Dau, H. (2012) Exptended protein/water H-bond networks in photosynthetic water oxidation Biochim. Biophys. Acta 1817, 1177-1190
87. Linke, K. and Ho, F. M. (2013) Water in Photosystem II: Structural, functional, and mechanistic considerations Biochim. Biophys. Acta 1837, 14-32
88. Noguchi, T. (2007) FTIR Detection of Water Reactions in the Oxygen-Evolving Center of Photosystem II Philos. Trans. R. Soc. London, Ser. B 363, 1189-1195