On the structure of the manganese complex of photosystem II: Extended-range EXAFS data and specific atomic-resolution models for four S-states

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1494, 2008, Pages 1237-1244

  Dau, Holger ^a   Grundmeier, Alexander ^a   Loja, Paola ^a   Haumann, Michael ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Photosynthesis; Photosynthetic oxygen evolution; Water oxidation; X ray absorption spectroscopy

Indexed keywords

AMINO ACID; ATOMIC ABSORPTION SPECTROSCOPY; COMPARATIVE STUDY; MANGANESE; OXIDATION; OXYGEN; PHOTOSYNTHESIS; PROTEIN; WATER; X-RAY SPECTROSCOPY;

EID: 38949209552     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.2220     Document Type: Article

References (40)

1. Chu, H. A., Hillier, W. & Debus, R. J. 2004 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 43, 3152-3166. (doi:10.1021/bi035915f)
2. Cinco, R. M., Holman, K. L. M., Robblee, J. H., Yano, J., Pizarro, S. A., Bellacchio, E., Sauer, K. & Yachandra, V. K. 2002 Calcium EXAFS establishes the Mn-Ca cluster in the oxygen-evolving complex of photosystem II. Biochemistry 41, 12 928-12 933. (doi:10.1021/bi026569p)
3. 4Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of photosystem II membranes. Biochemistry 43, 13 271-13 282. (doi:10.1021/bi036308v)
4. Crowley, J. D., Traynor, D. A., Weatherburn, D. C. 2000 Enzymes and proteins containing manganese: an overview. In Metal ions in biological systems: manganese and its role in biological systems, vol. 37, (eds A. Sigel & H. Sigel) pp. 279-304. New York, NY: Marcel Dekker.
5. Dau, H. & Haumann, M. 2006 Reaction cycle of photosynthetic water oxidation in plants and cyanobacteria. Science 312, 1471-1472.
6. Dau, H. & Haumann, M. 2007 Eight steps preceding O-O bond formation in oxygenic photosynthesis - a basic reaction cycle of the photosystem II manganese complex. Biochim. Biophys. Acta 1767, 472-483. (doi:10.1016/j.bbabio.2007.02.022)
7. Dau, H. & 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. (doi:10.1016/j.ccr.2007.09. 001)
8. Dau, H., Iuzzolino, L. & Dittmer, J. 2001 The tetramanganese complex of photosystem II during its redox cycle: X-ray absorption results and mechanistic implications. Biochim. Biophys. Acta 1503, 24-39. (doi:10.1016/S0005-2728(00)00230-9)
9. Dau, H., Liebisch, P. & Haumann, M. 2003 X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers - potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Anal. Bioanal. Chem. 376, 562-583. (doi:10.1007/s00216-003-1982-2)
10. 1-state: EXAFS results in relation to recent crystallographic data. Phys. Chem. Chem. Phys. 6, 4781-4792. (doi:10.1039/b408146c)
11. 3 transitions in photosystem II. Biochemistry 44, 1367-1374. (doi:10.1021/bi047558u)
12. Dittmer, J. & Dau, H. 1998 Theory of the linear dichroism in the extended X-ray absorption fine structure (EXAFS) of partially vectorially ordered systems. J. Phys. Chem. B 102, 8196-8200. (doi:10.1021/jp981049i)
13. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. 2004 Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838. (doi:10.1126/science.1093087)
14. Grabolle, M., Haumann, M., Muller, C., Liebisch, P. & Dau, H. 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. (doi:10.1074/jbc.M509724200)
15. Gu, W. et al. 2003 Refinement of the nickel site structure in Desulfovibrio gigas hydrogenase using range-extended EXAFS spectroscopy. J. Inorg. Biochem. 93, 41-51. (doi:10.1016/S0162-0134(02)00494-4)
16. 0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44, 1894-1908. (doi:10.1021/bi048697e)
17. 1 state in Cl-depleted and Br-reconstituted oxygen-evolving photosystem II: evidence from X-ray absorption spectroscopy at the Br K-edge. Biochemistry 45, 13 101-13 107. (doi:10.1021/bi061308r)
18. 3 transitions of the water oxidation cycle. Biochemistry 37, 17 112-17 119. (doi:10.1021/bi9817360)
19. Loll, B., Kern, J., Saenger, W., Zouni, A. & Biesiadka, J. 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040-1044. (doi:10.1038/nature04224)
20. Lundberg, M. & Siegbahn, P. E. M. 2004 Theoretical investigations of structure and mechanism of the oxygen-evolving complex in PSII. Phys. Chem. Chem. Phys. 6, 4772-4780. (doi:10.1039/b406552b)
21. 2 states. Biochem. J. 285, 569-576.
22. McEvoy, J. P. & Brudvig, G. W. 2006 Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483. (doi:10.1021/cr0204294)
23. Meinke, C., Sole, V. A., Pospisil, P. & Dau, H. 2000 Does the structure of the water-oxidizing photosystem II-manganese complex at room temperature differ from its low-temperature structure? A comparative X-ray absorption study. Biochemistry 39, 7033-7040. (doi:10.1021/ bi9924258)
24. Mishra, A., Wernsdorfer, W., Abboud, K. A. & Christou, G. 2005 The first high oxidation state manganese-calcium cluster: relevance to the water oxidizing complex of photosynthesis. Chem. Commun. (Camb.) 54-56. (doi:10.1039/b413680b)
25. Mukhopadhyay, S., Gandhi, B. A., Kirk, M. L. & Armstrong, W. H. 2003 A new class of oxo-bridged high-valent hexamanganese clusters supported by sterically hindered carboxylate ligands. Inorg. Chem. 42, 8171-8180. (doi:10.1021/ic034641h)
26. Mukhopadhyay, S., Mandal, S. K., Bhaduri, S. & Armstrong, W. H. 2004 Manganese clusters with relevance to photosystem II. Chem. Rev. 104, 3981-4026. (doi:10.1021/cr0206014)
27. Müller, C., Liebisch, P., Barra, M., Dau, H. & Haumann, M. 2005 The location of calcium in the manganese complex of oxygenic photosynthesis studied by X-ray absorption spectroscopy at the Ca K-edge. Phys. Script. T 115, 847-850. (doi:10.1238/Physica.Topical.115a00847)
28. 2 complex in response to a temperature jump: a time-resolved structural investigation employing X-ray absorption spectroscopy. Biophys. J. 84, 1370-1386.
29. Post, J. E. 1999 Manganese oxide minerals: crystal structures and economic and environmental significance. Proc. Natl Acad. Sci. USA 96, 3447-3454. (doi:10.1073/pnas.96.7.3447)
30. 4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy. J. Biol. Chem. 282, 7198-7208. (doi:10.1074/jbc.M610505200)
31. Rehr, J. J., Mustre de Leon, J., Zabinsky, S. I. & Albers, R. C. 1991 Theoretical X-ray absorption fine structure standards. J. Am. Chem. Soc. 113, 5135-5140. (doi:10.1021/ja00014a001)
32. 2 precipitates in the early ocean. Proc. Natl Acad. Sci. USA 99, 8631-8636. (doi:10.1073/pnas.132266199)
33. 2-state multiline signal by X-band EPR spectroscopy. J. Photochem. Photobiol. B 55, 138-144. (doi:10.1016/S1011-1344(00)00036-1)
34. Schiller, H., Dittmer, J., Iuzzolino, L., Dörner, W., Meyer-Klaucke, W., Sole, V. A., Nolting, H.-F. & Dau, H. 1998 Structure and orientation of the oxygen-evolving manganese complex of green algae and higher plants investigated by X-ray absorption linear dichroism spectroscopy on oriented photosystem II membrane particles. Biochemistry 37, 7340-7350. (doi:10.1021/bi972329b)
35. 3 transitions in photosystem II. Biochemistry 45, 8801-8811. (doi:10.1021/ bi060583a)
36. 3 transitions in photosystem II. Biochemistry 46, 3151-3160. (doi:10.1021/bi062195e)
37. 4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc. Natl Acad. Sci. USA 102, 12 047-12 052. (doi:10.1073/pnas.0505207102)
38. 4Ca cluster. J. Am. Chem. Soc. 127, 14 974-14 975. (doi:10.1021/ja054873a)
39. 4Ca cluster. Science 314, 821-825. (doi:10.1126/science.1128186)
40. Zouni, A., Witt, H. T., Kern, J., Fromme, P., Krauss, N., Saenger, W. & Orth, P. 2001 Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739-743. (doi:10.1038/35055589)