PH optimum of the photosystem II H2O oxidation reaction: Effects of PsbO, the manganese-stabilizing protein, Cl- retention, and deprotonation of a component required for O2 evolution activity

Biochemistry

Volumn 51, Issue 18, 2012, Pages 3808-3818

  Commet, Alan ^a,b   Boswell, Nicholas ^a   Yocum, Charles F ^a   Popelka, Hana ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; AMINO ACID RESIDUES; BINDING PROPERTIES; HYDROXIDE IONS; OXIDATION REACTIONS; PH OPTIMA; PHOTOSYSTEM II; PHOTOSYSTEM II ACTIVITIES; REACTION CENTER;

AMINO ACIDS; BINDING ENERGY; BINDING SITES; MANGANESE; PH EFFECTS;

CHLORINE COMPOUNDS;

CHLORINE; MUTANT PROTEIN; OXYGEN; PSBO PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; WATER;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEPROTONATION; MOLECULAR EVOLUTION; OXIDATION; PH; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTON TRANSPORT; STEADY STATE;

CHLORIDES; HYDROXIDES; OXIDATION-REDUCTION; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; SPINACIA OLERACEA;

EUKARYOTA;

EID: 84860744423     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201678m     Document Type: Article

References (82)

1. Nelson, N. and Yocum, C. F. (2006) Structure and function of photosystems I and II Annu. Rev. Plant Biol. 57, 521-565 (Pubitemid 44061036)
2. McConnell, I. L. (2008) Substrate water binding and oxidation in photosystem II Photosynth. Res. 98, 261-276 (Pubitemid 50260229)
3. Roose, J. L., Wegener, K. M., and Pakrasi, H. B. (2007) The extrinsic proteins of photosystem II Photosynth. Res. 92, 369-387 (Pubitemid 47246537)
4. Enami, I., Okumura, A., Nagao, R., Suzuki, T., Iwai, M., and Shen, J.-R. (2008) Structures and functions of the extrinsic proteins of photosystem II from different species Photosynth. Res. 98, 349-363 (Pubitemid 50247998)
5. Lydakis-Simantiris, N., Hutchison, R. S., Betts, S. D., Barry, B. A., and Yocum, C. F. (1999) Manganese stabilizing protein of photosystem II is a thermostable, natively unfolded polypeptide Biochemistry 38, 404-414 (Pubitemid 29035711)
6. Popelkova, H., Wyman, A., and Yocum, C. F. (2003) Amino acid sequences and solution structures of manganese stabilizing protein that affect reconstitution of photosystem II activity Photosynth. Res. 77, 21-34 (Pubitemid 37078105)
7. Williamson, A. K. (2008) Structural and functional aspects of the MSP (PsbO) and study of its differences in thermophilic versus mesophilic organisms Photosynth. Res. 98, 365-389 (Pubitemid 50266022)
8. Popelkova, H. and Yocum, C. F. (2011) PsbO, the manganese-stabilizing protein: Analysis of the structure-function relations that provide insights into its role in photosystem II J. Photochem. Photobiol., B 104, 179-190
9. Popelkova, H., Commet, A., and Yocum, C. F. (2010) The double mutant ΔL6MW241F in PsbO, the photosystem II manganese stabilizing protein, yields insights into the evolution of its structure and function FEBS Lett. 584, 4009-4014
10. van Gorkom, H. J. and Yocum, C. F. (2005) The Calcium and Chloride Cofactors. In Photosystem II: The Light Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T. J. and Satoh, K., Eds.) pp 307-328, Springer, Dordrecht, The Netherlands.
11. - ion in the oxygen-evolving complex Photosynth. Res. 93, 111-121 (Pubitemid 47310275)
12. Sandusky, P. O. and Yocum, C. F. (1983) The mechanism of amine inhibition of the photosynthetic oxygen evolving complex: Amines displace functional chloride form a ligand site on manganese FEBS Lett. 162, 339-343
13. Britt, R. D. (2004) Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: Implications as to water oxidation mechanisms Biochim. Biophys. Acta 1655, 158-171 (Pubitemid 38526176)
14. Vrettos, J. S., Limburg, J., and Brudvig, G. W. (2001) Mechanism of photosynthetic water oxidation: Combining biophysical studies of photosystem II with inorganic model chemistry Biochim. Biophys. Acta 1503, 229-245
15. Ono, T., Zimmermann, J. L., Inoue, T., and Rutherford, A. W. (1986) EPR evidence for a modified S-state transition in chloride-depleted photosystem II Biochim. Biophys. Acta 851, 193-201
16. 2 transitions Biochemistry 36, 3663-3670 (Pubitemid 27143522)
17. Boussac, A. and Rutherford, A. W. (1994) Electron transfer events in chloride-depleted photosystem II J. Biol. Chem. 269, 12462-12467 (Pubitemid 24202026)
18. Olesen, K. and Andréasson, L.-E. (2003) The function of the chloride ion in photosynthetic oxygen evolution Biochemistry 42, 2025-2035 (Pubitemid 36258676)
19. McEvoy, J. P. and Brudvig, G. W. (2004) Structure-based mechanism of photosynthetic water oxidation Phys. Chem. Chem. Phys. 6, 4754-4763
20. McEvoy, J. P., Gascon, J. A., Batista, V. S., and Brudvig, G. W. (2005) The mechanism of photosynthetic water splitting Photochem. Photobiol. Sci. 4, 940-949 (Pubitemid 41818863)
21. Murray, J. W., Maghlaoui, K., Kargul, J., Ishida, N., Lai, T.-L., Rutherford, A. W., Sugiura, M., Boussac, A., and Barber, J. (2008) X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of photosystem II Energy Environ. Sci. 1, 161-166
22. Kawakami, K., Umena, Y., Kamiya, N., and Shen, J.-R. (2009) Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography Proc. Natl. Acad. Sci. U.S.A. 106, 8567-8572
23. 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 Nat. Struct. Mol. Biol. 16, 334-342
24. Pokhrel, R., McConnell, I. L., and Brudvig, G. (2011) Chloride regulation of enzyme turnover: Application of the role of chloride in photosystem II Biochemistry 50, 2725-2734
25. Rivalta, I., Amin, M., Luber, S., Vassiliev, S., Pokhrel, R., Umena, Y., Kawakami, K., Shen, J.-R., Kamiya, N., Bruce, D., Brudvig, G. W., Gunner, M. R., and Batista, V. S. (2011) Structural-functional role of chloride in photosystem II Biochemistry 50, 6312-6315
26. 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 angstrom resolution Nature 409, 739-743 (Pubitemid 32144521)
27. 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 (Pubitemid 36078036)
28. 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 (Pubitemid 38374869)
29. 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 (Pubitemid 43093979)
30. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosytem II at a resolution of 1.9 Å Nature 473, 55-60
31. Brosser, M., Glöckner, C., Gabdulkhakov, A., Guzkov, A., Buchta, J., Kern, J., Müh, F., Dau, H., Saenger, W., and Zouni, A. (2011) Structural basis of cyanobacterial photosystem II inhibition by the herbicide Terbutryn J. Biol. Chem. 286, 15964-15972
32. 4Ca cluster J. Am. Chem. Soc. 127, 14974-14975 (Pubitemid 41547334)
33. 2-evolving complex of photosystem II Biochemistry 50, 6308-6311
34. 2 evolving complex of photosystem II Biochemistry 37, 8595-8604 (Pubitemid 28275478)
35. Kelly, 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 Biochim. Biophys. Acta 502, 198-210 (Pubitemid 8326463)
36. Homann, P. H. (1988) The chloride and calcium requirements of photosynthetic water oxidation: Effects of pH Biochim. Biophys. Acta 934, 1-13
37. Miyao, M. and Murata, M. (1984) Effect of urea on photosystem II particles. Evidence for an essential role of the 33 kDa polypeptide in photosynthetic oxygen evolution Biochim. Biophys. Acta 765, 253-257
38. Bricker, T. M. (1992) Oxygen evolution in the absence of the 33 kDa manganese-stabilizing protein Biochemistry 31, 4623-4628
39. Miyao, M. and Murata, M. (1984) Role of the 33-kDa polypeptide in preserving Mn in the photosynthetic oxygen-evolution system and its replacement by chloride ions FEBS Lett. 170, 350-354
40. Kuwabara, T., Miyao, M., Murata, T., and Murata, N. (1985) The function of 33-kDa protein in the photosynthetic oxygen-evolution system studied by reconstitution experiments Biochim. Biophys. Acta 806, 283-289
41. Popelkova, H., Commet, A., Kuntzleman, T., and Yocum, C. F. (2008) Inorganic cofactor stabilization and retention: The unique functions of the two PsbO subunits of eukaryotic photosystem II Biochemistry 47, 12593-12600
42. Popelkova, H., Betts, S. D., Lydakis-Simantiris, N., Im, M. M., Swenson, E., and Yocum, C. F. (2006) Mutagenesis of basic residues R151 and R161 in manganese-stabilizing protein of photosystem II causes inefficient binding of chloride to the oxygen-evolving complex Biochemistry 45, 3107-3115 (Pubitemid 43334559)
43. Popelkova, H., Commet, A., and Yocum, C. F. (2009) Asp157 is required for the function of PsbO, the photosystem II manganese-stabilizing protein Biochemistry 48, 11920-11928
44. Sandusky, P. O., Selvius DeRoo, C. L., Hicks, D. B., Yocum, C. F., Ghanotakis, D. F., and Babcock, G. T. (1983) Electron Transport Activity and Polypeptide Composition of the Isolated Photosystem II Complex. In The Oxygen Evolving System of Photosynthesis (Inoue, Y., Crofts, A. R., Govindjee, Murata, N., Renger, G., and Satoh, K., Eds.) pp 189-199, Academic Press, Tokyo.
45. 2-state multiline signal by X-band EPR spectroscopy J. Photochem. Photobiol., B 55, 138-144 (Pubitemid 30440482)
46. 2 evolution by thylakoids from salt-tolerant higher plant Biochim. Biophys. Acta 682, 436-445
47. 2 Evolving Centers. In The Oxygen Evolving System of Photosynthesis (Inoue, Y., Crofts, A. R., Govindjee, Murata, N., Renger, G., and Satoh, K., Eds.) pp 293-302, Academic Press, Tokyo.
48. 2 state in chloride-depleted water oxidizing complexes after reconstituting treatments with various monovalent anions Photosynth. Res. 38, 395-400
49. van Vliet, P. and Rutherford, A. W. (1996) Properties of the chloride-depleted oxygen-evolving complex of photosystem II studied by electron paramagnetic resonance Biochemistry 35, 1829-1839 (Pubitemid 26062632)
50. 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 Biochim. Biophys. Acta 766, 603-611
51. Haddy, A., Hatchell, J. A., Kimel, R. A., and Thomas, R. (1999) Azide as a competitor of chloride in oxygen evolution by photosystem II Biochemistry 38, 6104-6110
52. Kühne, H., Szalai, V. A., and Brudvig, G. W. (1999) Competitive binding of acetate and chloride in photosystem II Biochemistry 38, 6604-6613
53. 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, 12022-12029 (Pubitemid 41285699)
54. 2-State multiline signal ESEEM study J. Am. Chem. Soc. 124, 10921-10933
55. Popelkova, H., Im, M. M., D'Auria, J., Betts, S. D., Lydakis-Simantiris, N., and Yocum, C. F. (2002) N-terminus of the photosystem II manganese stabilizing protein: Effects of sequence elongation and truncation Biochemistry 41, 2702-2711 (Pubitemid 34168939)
56. Popelkova, H., Im, M. M., and Yocum, C. F. (2002) N-terminal truncations of manganese stabilizing protein identify two amino acid sequences required for binding of the eukaryotic protein to photosystem II and reveal the absence of one binding-related sequence in cyanobacteria Biochemistry 41, 10038-10045 (Pubitemid 34839750)
57. Popelkova, H., Im, M. M., and Yocum, C. F. (2003) Binding of manganese stabilizing protein to photosystem II: Identification of essential N-terminal threonine residues and domains that prevent nonspecific binding Biochemistry 42, 6193-6200 (Pubitemid 36605121)
58. Roose, J. L., Yocum, C. F., and Popelkova, H. (2011) Binding stoichiometry and affinity of the manganese-stabilizing protein affects redox reactions on the oxidizing side of photosystem II Biochemistry 50, 5988-5998
59. Vass, I., Koike, H., and Inoue, Y. (1985) High pH effect on S-state turnover in chloroplasts studied by thermoluminescence. Short-time alkaline incubation reversibly inhibits S3-to-S4 transition Biochim. Biophys. Acta 810, 302-309
60. Kuwabara, T. and Murata, N. (1983) Quantitative analysis of the inactivation of photosynthetic oxygen evolution and the release of polypeptides and manganese in the photosystem II particles of spinach chloroplasts Plant Cell Physiol. 24, 741-747
61. Weast, R. C. and Astle, M. J. (1978) CRC Handbook of Chemistry and Physics, 59th ed., pp D-204, CRC Press, Inc., Boca Raton, FL.
62. Sandusky, P. O. and Yocum, C. F. (1986) The chloride requirement for photosynthetic oxygen evolution: Factors affecting nucleophilic displacement of chloride from the oxygen-evolving complex Biochim. Biophys. Acta 849, 85-93
63. Miyao, M., Murata, N., Lavorel, J., Maison-Peteri, B., Boussac, A., and Etienne, A.-L. (1987) Effect of the 33-kDa protein on the S-state transitions in photosynthetic oxygen evolution Biochim. Biophys. Acta 890, 151-159
64. Burnap, R. L., Shen, J.-R., Jursinic, P. A., Inoue, Y., and Sherman, L. A. (1992) Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese-stabilizing protein of photosystem II Biochemistry 31, 7404-7410
65. Roose, J. L., Yocum, C. F., and Popelkova, H. (2010) Function of PsbO, the photosystem II manganese-stabilizing protein: Probing the role of Asp157 Biochemistry 49, 6042-6051
66. 448Ser mutant in the CP47 protein of photosystem II under normal and low chloride conditions Biochemistry 40, 11483-11489 (Pubitemid 32911290)
67. 444R Biochemistry 35, 4046-4053
68. Young, A., McChargue, M., Frankel, L. K., Bricker, T. M., and Putnam-Evans, C. (2002) Alterations of the oxygen-evolving apparatus induced by a (305)Arg → (305)Ser mutation in the CP43 protein of photosystem II from Synechocystis sp. PCC 6803 under chloride-limiting conditions Biochemistry 41, 15747-15753 (Pubitemid 36062479)
69. Rosenberg, C., Christian, J., Bricker, T. M., and Putnam-Evans, C. (1999) Site-directed mutagenesis of glutamate residues in the large extrinsic loop of the photosystem II protein CP43 affects oxygen-evolving activity and PSII assembly Biochemistry 38, 15994-16000 (Pubitemid 129520494)
70. Segel, I. H. (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, pp 893-898, John Wiley and Sons, Inc., New York.
71. 2+ J. Chin. Chem. Soc. 51, 1221-1228 (Pubitemid 44076534)
72. Creighton, T. E. (1993) Proteins: Structures and Molecular Properties, W. H. Freeman and Co., New York.
73. Pétra, P. H. and Neurath, H. (1971) Modification of carboxyl groups in bovine carboxypeptidase A. II. Chemical identification of a functional glutamic acid residue and other reactive groups Biochemistry 10, 3171-3177
74. Kokesh, F. C. and Westheimer, F. H. (1971) A reporter group at the active site of acetoacetate decarboxylase. II. Ionization constant of the amino group J. Am. Chem. Soc. 93, 7270-7274
75. Ploegman, J. H., Drent, G., Kalk, K. H., and Hol, W. G. J. (1979) The structure of bovine liver rhodanese J. Mol. Biol. 127, 149-162
76. Lewis, S. D., Johnson, F. A., and Shafer, J. A. (1981) Effect of cysteine-25 on the inonizaiton of His-159 in papain as determined by proton nuclear magnetic resonance spectroscopy. Evidence for a His-159-Cys-25 ion pair and its possible role in catalysis Biochemistry 20, 48-51
77. Nyarko, A., Cochrun, L., Norwood, S., Pursifull, N., Voth, A., and Barbar, E. (2005) Ionization of His 55 at the dimer interface of dynein light-chain LC8 is coupled to dimer dissociation Biochemistry 44, 14248-14255 (Pubitemid 41533049)
78. Khandogin, J. and Brooks, C. L., III (2006) Toward the accurate first-principle prediction of ionization equilibria in proteins Biochemistry 45, 9363-9373 (Pubitemid 44223241)
79. 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 (Pubitemid 43271306)
80. 4 cluster in photosystem II based on solvent accessibility simulations, with implications for substrate water access Biochim. Biophys. Acta 1777, 140-153 (Pubitemid 351187745)
81. Lindberg, K., Vänngård, T., and Andréasson, L.-E. (1993) Studies of the slowly exchanging chloride in photosystem II Photosynth. Res. 38, 401-408
82. 4Ca cluster of photosystem II involving D1-Glu65, D2-Glu312, and D1-Glu329 Biochemistry 49, 6655-6669