Calcium exchange and structural changes during the photosynthetic oxygen evolving cycle

Biophysical Journal

Volumn 91, Issue 5, 2006, Pages 1999-2008

  De Riso, Antonio ^a   Jenson, David L ^a   Barry, Bridgette A ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHLORIDE; MANGANESE; OXYGEN; STRONTIUM;

ARTICLE; CALCIUM TRANSPORT; MEDICAL RESEARCH; PHOTOOXIDATION; PHOTOSYNTHESIS; SPECTROSCOPY;

EID: 33748441390     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.087171     Document Type: Article

References (75)

1. Joliot, P., and B. Kok. 1975. Oxygen evolution in photosynthesis. In Bioenergetics of Photosynthesis. Govindjee, editor. Academic Press, New York. 388-412.
2. Britt, R. D., K. A. Campbell, J. M. Peloquin, M. L. Gilchrist, C. P. Aznar, M. M. Dicus, J. Robblee, and J. Messinger. 2004. Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta. 1655:158-171.
3. Ono, T., T. Noguchi, Y. Inoue, M. Kusunoki, T. Matsushita, and H. Oyanagi. 1992. X-ray detection of the period-four cycling of the manganese cluster in photosynthetic water oxidizing enzyme. Science. 258:1335-1337.
4. 2 formation tracked by time-resolved x-ray experiments. Science. 310:1019-1021.
5. Roelofs, T. A., W. Liang, M. L. Latimer, R. M. Cinco, A. Rompel, J. C. Andrews, K. Sauer, V. K. Yachandra, and M. P. Klein. 1996. Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex. Proc. Natl. Acad. Sci. USA. 93:3335-3340.
6. 3 transition: implications for the mechanism of photosynthetic water oxidation. J. Am. Chem. Soc. 123:7804-7820.
7. 2 state: determination by x-ray absorption spectroscopy. Biochemistry. 33:4923-4932.
8. 2O. Biochemistry. 36:8904-8913.
9. 3 state transition of the oxygen-evolving complex of photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn x-ray absorption spectroscopy. J. Am. Chem. Soc. 122:3399-3412.
10. Yocum, C. F. 1992. The calcium and chloride requirements for photosynthetic water oxidation. In Manganese Redox Enzymes. V. L. Pecoraro, editor. VCH Publishers, New York. 71-83.
11. Penner-Hahn, J. E., R. M. Fronko, V. L. Pecoraro, C. F. Yocum, S. D. Betts, and N. R. Bowlby. 1990. Structural characterization of the manganese sites in the photosynthetic oxygen-evolving complex using x-ray absorption spectroscopy. J. Am. Chem. Soc. 112:2549-2557.
12. Latimer, M. J., V. J. DeRose, V. K. Yachandra, K. Sauer, and M. P. Klein. 1998. Structural effects of calcium depletion on the manganese cluster of photosystem II: determination by x-ray absorption spectroscopy. J. Phys. Chem. B. 102:8257-8265.
13. 87Sr ESEEM spectroscopy. J. Am. Chem. Soc. 126:7228-7237.
14. Zouni, A., H.-T. Witt, J. Kern, P. Fromme, N. Krauß, W. Saenger, and P. Orth. 2001. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature. 409:739-743.
15. Kamiya, N., and J.-R. Shen. 2003. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc. Natl. Acad. Sci. USA. 100:98-103.
16. Ferreira, K. N., T. M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata. 2004. Architecture of the photosynthetic oxygen-evolving center. Science. 303:1831-1837.
17. Loll, B., J. Kern, W. Saenger, A. Zouni, and J. Biesiadka. 2005. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature. 438:1040-1044.
18. 4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography. Proc. Natl. Acad. Sci. USA. 102:12047-12052.
19. Grabolle, M., M. Haumann, C. Muller, P. Liebisch, and H. Dau. 2006. Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K. J. Biol. Chem. 281:4580-4588.
20. 113Cd NMR. Biochemistry. 39:6751-6755.
21. Ghanotakis, D. F., G. T. Babcock, and C. F. Yocum. 1984. Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted photosystem II preparations. FEBS Lett. 167:127-130.
22. +2-deficient photosystem II. Biochemistry. 28:8984-8989.
23. +2 substitution on the reduction rates of YzΣ in PSII membranes - evidence for concerted hydrogen-atom transfer in oxygen evolution. Biochemistry. 39:16220-16229.
24. +2 exchange in photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus. J. Biol. Chem. 279:22809-22819.
25. Riggs-Gelasco, P. J., R. Mei, C. F. Yocum, and J. E. Penner-Hahn. 1996. Reduced derivatives of the Mn cluster in the oxygen-evolving complex of photosystem II: an EXAFS study. J. Am. Chem. Soc. 118:2387-2399.
26. Haumann, M., and W. Junge. 1999. Photosynthetic water oxidation: a simplex-scheme of its partial reactions. Biochim. Biophys. Acta. 1411:86-91.
27. Barry, B. A., C. Hicks, A. De Riso, and D. L. Jenson. 2005. Calcium ligation in photosystem II under inhibiting conditions. Biophys. J. 89:393-401.
28. Pecoraro, V. L., M. J. Baldwin, M. T. Caudle, W. Y. Hsieh, and N. A. Law. 1998. A proposal for water oxidation in photosystem II. Pure Appl. Chem. 70:925-929.
29. 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in photosystem II. Biochemistry. 42:6209-6217.
30. 2 formation. Biochemistry. 40:7937-7945.
31. Barry, B. A., I. B. Cooper, A. De Riso, S. H. Brewer, D. Vu, and R. B. Dyer. 2006. Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle. Proc. Natl. Acad. Sci. USA. 103:7288-7291.
32. Hillier, W., and G. Babcock. 2001. S-state dependent Fourier transform infrared difference spectra for the photosystem II oxygen evolving complex. Biochemistry. 40:1503-1509.
33. Noguchi, T., T. Tomo, and C. Kato. 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.
34. Yamanari, T., Y. Kimura, N. Mizusawa, A. Ishii, and T. Ono. 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.
35. 13C isotope labeling. Biochemistry. 42:6035-6042.
36. Sachs, R., K. M. Halverson, and B. A. Barry. 2003. Specific isotope labeling and photooxidation-linked structural changes in the manganese stabilizing subunit of photosystem II. J. Biol. Chem. 278:44222-44229.
37. Strickler, M. A., L. M. Walker, W. Hillier, and R. J. Debus. 2005. Evidence from biosynthetically incorporatted strontium and FTIR difference spectroscopy that the C-terminus of the D1 polypeptide of photosystem II does not ligate calcium. Biochemistry. 44:8571-8577.
38. Berthold, D. A., G. T. Babcock, and C. F. Yocum. 1981. A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett. 134:231-234.
39. Anderson, L. B., A. J. A. Ouellette, and B. A. Barry. 2000. Probing the primary structure of photosystem II with amines and phenylhydrazine. J. Biol. Chem. 275:4920-4927.
40. +2 on the oxidizing side of photosystem II. FEBS Lett. 170:169-173.
41. Barry, B. A. 1995. Tyrosyl radicals in photosystem II. Methods Enzymol. 258:303-319.
42. Yocum, C. F. 1991. Calcium activation of photosynthetic water oxidation. Biochim. Biophys. Acta. 1059:1-15.
43. Halverson, K. M., and B. A. Barry. 2003. Evidence for spontaneous structural changes in a dark-adapted state of photosystem II. Biophys. J. 85:2581-2588.
44. Halverson, K. M., and B. A. Barry. 2003. Sucrose and glycerol effects on photosystem II. Biophys. J. 85:1317-1325.
45. Kim, S., and B. A. Barry. 1998. The protein environment surrounding tyrosyl radicals DΣ and ZΣ in photosystem II: a difference FT-IR study. Biophys. J. 74:2588-2600.
46. Miller, A.-F., and G. W. Brudvig. 1991. A guide to electron paramagnetic resonance spectroscopy of photosystem II membranes. Biochim. Biophys. Acta. 1056:1-18.
47. Krimm, S., and J. Bandekar. 1986. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. In Advances in Protein Chemistry. Vol. 38. C. B. Anfinsen, J. T. Edsall, and F. M. Richards, editors. Academic Press, New York. 181-364.
48. Braiman, M. S., D. M. Briercheck, and K. M. Kriger. 1999. Modeling vibrational spectra of amino acid side chains in proteins: effects of protonation state, counterion, and solvent on arginine C-N stretch frequencies. J. Phys. Chem. B. 103:4744-4750.
49. Kimura, Y., N. Mizusawa, A. Ishii, and T.-a. Ono. 2005. FTIR detection of structural changes in a histidine ligand during S-state cycling of photosynthetic oxygen-evolving complex. Biochemistry. 44:16072-16078.
50. 3 transitions in photosystem II. Biochemistry. 44:1367-1374.
51. Dekker, J. P., J. J. Plijter, L. Ouwehand, and H. J. van Gorkom. 1984. Kinetics of manganese redox transitions in the oxygen-evolving apparatus of photosynthesis. Biochim. Biophys. Acta. 767:176-179.
52. 2-evolving complex of photosystem II. Biochemistry. 24:3035-3043.
53. Steenhuis, J. J., and B. A. Barry. 1996. A difference infrared study of protein structural changes in the photosynthetic water-oxidizing complex. J. Am. Chem. Soc. 118:11927-11932.
54. 2 state in photosynthetic oxygen evolution: a difference FT-IR study. J. Phys. Chem. 101:6652-6660.
55. Steenhuis, J. J., and B. A. Barry. 1998. An FT-IR study of photoassembly in the manganese catalytic site of photosystem II. J. Phys. Chem. 102:4-8 [Letter].
56. Hutchison, R. S., J. J. Steenhuis, C. F. Yocum, R. M. Razeghifard, and B. A. Barry. 1999. Deprotonation of the 33 kDa, extrinsic, manganese stabilizing protein accompanies photooxidation of manganese in photosystem II. J. Biol. Chem. 274:31987-31995.
57. Boerner, R. J., A. P. Nguyen, B. A. Barry, and R. J. Debus. 1992. Evidence from directed mutagenesis that aspartate 170 of the D1 polypeptide influences the assembly and/or stability of the manganese cluster in the photosynthetic water-splitting complex. Biochemistry. 31:6660-6672.
58. Steenhuis, J. J., R. S. Hutchison, and B. A. Barry. 1999. Alternations in carboxylate ligation at the active site of photosystem II. J. Biol. Chem. 274:14609-14616.
59. Smith, J. C., E. Gonzalez-Vergara, and J. B. Vincent. 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.
60. Phillips, G. N., Jr., M. L. Teodoro, T. Li, B. Smith, and J. S. Olson. 1999. Bound CO is a molecular probe of electrostatic potential in the distal pocket of myoglobin. J. Phys. Chem. B. 103:8817-8829.
61. Suydam, I. T., and S. G. Boxer. 2003. Vibrational Stark effects calibrate the sensitivity of vibrational probes for electric fields in proteins. Biochemistry. 42:12050-12055.
62. McEvoy, J. P., and G. W. Brudvig. 2004. Structure-based mechanism of photosynthetic water oxidation. Phys. Chem. Chem. Phys. 6:4754-4763.
63. 113Cd NMR studies of the chelation of metal ions by the calcium binding protein parvalbumin. J. Inorg. Biochem. 25:141-149.
64. Szebenyi, D. M., and K. Moffat. 1986. The refined structure of vitamin D-dependent calcium-binding protein from bovine intestine. Molecular details, ion binding, and implications for the structure of other calcium-binding proteins. J. Biol. Chem. 261:8761-8777.
65. Ilag, L. L., R. McKenna, M. P. Yadav, J. N. BeMiller, N. L. Incardona, and M. G. Rossmann. 1994. Calcium ion-induced structural changes in bacteriophage phi X174. J. Mol. Biol. 244:291-300.
66. Dudev, T., Y. Lin, M. Dudev, and C. Lim. 2003. First-second shell interactions in metal binding sites in proteins: a PDB survey and DFT/CDM calculations. J. Am. Chem. Soc. 125:3168-3180.
67. Fox, B. A., V. C. Yee, L. C. Pedersen, I. L. Trong, P. D. Bishop, R. E. Stenkamp, and D. C. Teller. 1999. Identification of the calcium binding site and a novel yterrbium site in blood coagulation factor XIII by x-ray crystallography. J. Biol. Chem. 274:4917-4923.
68. Schauer, C. K., and O. P. Anderson. 1987. Calcium-selective ligands. 2. Structural and spectroscopic studies on calcium and cadmium complexes of EGTA. J. Am. Chem. Soc. 109:3646-3656.
69. Joris, S. J., and C. H. Amberg. 1971. The nature of deficiency in nonstoichiometric hydroxyapatites. II. Spectroscopic studies of calcium and strontium hydroxyapatites. J. Phys. Chem. 75:3172-3178.
70. Kashino, Y., W. M. Lauber, J. A. Carroll, Q. Wang, J. Whitmarsh, K. Satoh, and H. B. Pakrasi. 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.
71. +2 depletion and metal cation substitution in the photosyntheticc oxygen-evolving complex. Biochemistry. 41:5844-5853.
72. Nishikawa T., M. Murakami, and T. Kouyama. 2005. Crystal structure of the 13-cis isomer of bacteriorhodopsin in the dark-adapted state. J. Mol. Biol. 352:319-328.
73. Moody, A. J., C. E. Cooper, R. B. Gennis, J. N. Rumbley, and P. R. Rich. 1995. Interconversion of fast and slow forms of cytochrome bo from Escherichia coli. Biochemistry. 34:6838-6846.
74. Moody, A. J., C. E. Cooper, and P. R. Rich. 1991. Characterisation of 'fast' and 'slow' forms of bovine heart cytochrome-c oxidase. Biochim. Biophys. Acta. 1059:189-207.
75. Carey, F. A., and R. J. Sundberg. 2000. Advanced Organic Chemistry. Kluwer Academic/Plenum Publishers, New York.