Structural and EPR characterization of the soluble form of cytochrome c-550 and of the psbV2 gene product from the cyanobacterium Thermosynechococcus elongatus

Plant and Cell Physiology

Volumn 44, Issue 7, 2003, Pages 697-706

  Kerfeld, Cheryl A ^a   Sawaya, Michael R ^a   Bottin, Hervé ^b   Tran, Kimberlee T ^a   Sugiura, Miwa ^b   Cascio, Duilio ^a   Desbois, Alain ^b   Yeates, Todd O ^a   Kirilovsky, Diana ^b   Boussac, Alain ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEA SACLAY   (France)

Author keywords

Crystal structure; Cytochrome; EPR; Photosystem II; Resonance Raman; Thermophile

Indexed keywords

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLIZATION; CYANOBACTERIA; CYTOCHROME C GROUP; HEMEPROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBILITY; SPECTRUM ANALYSIS, RAMAN; ULTRAVIOLET RAYS;

ARTHROSPIRA MAXIMA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 0041696473     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pcg084     Document Type: Article

References (48)

1. Alam, J., Sprinkle, J.R., Hermodson, M.A. and Krogmann, D.W. (1984) Characterization of cytochrome c-550 from cyanobacteria. Biochim. Biophys. Acta 766: 317-321.
2. Boussac, A., Sugiura, M., Inoue, Y. and Rutherford, A.W. (2000) EPR study of the oxygen evolving complex in His-tagged photosystem II from the cyanobacterium Synechococcus elongatus. Biochemistry 39: 13788-13799.
3. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., Read, R.J., Rice, L.M., Simonson, T. and Warren, G.L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Cryst. D54: 905-921.
4. Collaborative Computational Project, Number 4 (1994) "The CCP4 Suite: Programs for Protein Crystallography". Acta Cryst. D50: 760-763.
5. Colovos, C.R. and Yeates, T.O. (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci. 2: 1511-1519.
6. Dalhus, B., Saarinen, M., Sauer, U.H., Eklund, P., Johansson, K., Karlsson, A., Ramaswamy, S., Bjork, A., Synstad, B., Naterstad, K., Sirevag, R. and Eklund, H. (2002) Structural basis for thermophilic protein stability: Structures of thermophilic and mesophilic malate dehydrogenases. J. Mol. Biol. 318: 707-721.
7. DeLano, W.L. (2002) The PyMOL Molecular Graphics System (available at http://www.pymol.org).
8. Desbois, A. (1994) Resonance Raman spectroscopy of c-type cytochromes. Biochimie 76: 693-707.
9. Döpner, S., Hildebrand, P., Rosell, F.I. and Mauk, A.G. (1998) alkaline conformational transitions of fericytochrome c studied by resonance Raman spectroscopy. J. Am. Chem. Soc. 120: 11246-11255.
10. Frazao, C., Enguita, F.J., Coelho, R., Sheldrick, G.M., Navarro, J.A., Hervas, M., De la Rosa M.A. and Carrondo, M.A. (2001) Crystal structure of low-potential cytochrome c(549) from Synechocystis sp PCC 6803 at 1.21 Ångstrom resolution. J. Biol. Inorg. Chem. 6: 324-332.
11. Ho, K.K., Ulrich, E.L., Krogmann, D.W. and Gomez-Lojero, C. (1979) Isolation of photosynthetic catalysts from cyanobacteria. Biochim. Biophys. Acta 545: 236-248.
12. Hoganson, C.W., Lagenfelt, G. and Andreasson, L. (1990) EPR and redox potentiometric studies of cytochrome c-549 of Anacystis nidulans. Biochim. Biophys. Acta 1016: 203-206.
13. Holton, R.W. and Myers, J. (1963) Cytochromes of a blue-green alga: Extraction of a c-type with a strongly negative redox potential. Science 142: 234-235.
14. Hu, S., Morris, I.K., Singh, J.P., Smith, K.M. and Spiro, T.G. (1993) Complete assignment of cytochrome c resonance Raman spectra via enzymatic reconstitution with isotopically labeled hemes. J. Am. Chem. Soc. 115: 12446-12458.
15. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A47: 110-119.
16. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W. and Krauss, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution. Nature 411: 909-917.
17. 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. USA 100: 98-103.
18. Kang, C., Chitnis, P.R., Smith, S. and Krogmann, D.W. (1994) Cloning and sequence analysis of the gene encoding the low potential cytochrome c of Synechocystis PCC 6803. FEBS Lett. 344: 5-9.
19. Katoh, H., Itoh, S., Shen, J.-R. and Ikeuchi, M. (2001) Functional analysis of psbV and a novel c-type cytochrome gene psbV2 of the thermophilic cyanobacterium Thermosynechococcus elongatus Strain BP-1. Plant Cell Physiol. 42: 599-607.
20. Kerfeld, C.A. and Krogmann, D.W. (1998) Photosynthetic cytochromes c in cyanobacteria, algae, and plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 397-425.
21. Kienzel, P.F. and Peschek, G.A. (1983) Cytochrome c-549: an endogenous cofactor of cyclic photophosphorylation in the cyanobacterium Anacystis nidulans. FEBS Lett. 162: 76-80.
22. Kitagawa, T., Kyogoku, Y., Iizuka, T., Ikeda-Saito, M. and Yamanaka, T. (1975) resonance Raman scattering from hemoproteins. Effects of ligands upon the Raman spectra of various c-type cytochromes. J. Biochem. 78: 719-728.
23. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
24. Lefevre-Groboillot, D., Dijols, S., Boucher, J.-L., Mahy, J.-P., Ricoux, R., Desbois, A., Zimmermann, J.-L. and Mansuy, D. (2001) N-hydroxyguanidines as new heme ligands: UV-visible, EPR, and resonance Raman studies of the interaction of various compounds bearing a C=NOH function with microperoxidase-8. Biochemistry 40: 9909-9917.
25. Morand, L.Z., Cheng, R.H. and Krogmann, D.W. (1994) Soluble electron transfer catalysts of cyanobacteria. In The Molecular Biology of Cyanobacteria. Edited by Bryant, D.A. pp. 243-269. Kluwer Academic, Dordrecht.
26. Nakamura, Y., Kaneko, T., Sato, S., Ikeuchi, M., Katoh, H., Sasamoto, S., Watanabe, A., Iriguchi, M., Kawashima K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M. and Tabata, S. (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. 9: 123-130.
27. Navarro, J.A., Hervas, M., De la Cerda, B. and De la Rosa, M.A. (1995) Purification and physicochemical properties of the low-potential cytochrome c549 from the cyanobacterium Synechocystis sp. PCC 6803. Arch. Biochem. Biophys. 318: 46-52.
28. Othman, S. and Desbois, A. (1998) Resonance Raman investigation of lysine and N-acetylmethionine complexes of ferric and ferrous microperoxidase. Influence of the axial ligation on the heme c structure. Eur. Biophys. J. 28: 12-25.
29. 2. A resonance Raman study. Biochemistry 36: 5499-5508.
30. Othman, S., Le Lirzin, A. and Desbois, A. (1994) Resonance Raman investigation of imidazole and imidazolate complexes of microperoxidase: characterization of the bis(histidine) axial ligation in c-type cytochromes. Biochemistry 33: 15437-15448.
31. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillating mode. Methods Enzymol. 276A: 307-326.
32. Palmer, G. (1985) The electron paramagnetic resonance of metalloproteins. Biochem. Soc. Trans. 13: 548-560.
33. Peisach, J., Blumberg, W.E. and Adler, A. (1973) Electron paramagnetic resonance studies of iron porphyrin and chlorin systems. Ann. N. Y. Acad Sci. 206: 310-327.
34. Perrakis, A., Morris, R. and Lamzin, V.S. (1999) Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6: 458-463.
35. Quin, R., Valentine, J.S., Byrn, M.P. and Strouse, C.E. (1987) Electronic structure of low-spin ferric porphyrins: A single-crystal EPR and structural investigation of the influence of axial ligands orientation and the effects of pseudo-Jahn-Teller distortion. J. Am. Chem. Soc. 109: 3301-3308.
36. Roncel, M., Boussac, A.M., Zurita, J.L., Bottin, H., Sugiura, M., Kirilovsky, D. and Ortega, J.-M. (2003) Redox properties of the photosystem II cytochromes b559 and c550 in the cyanobacterium Thermosynechococcus elongatus. J. Biol. Inorg. Chem. 8: 206-216.
37. Šali, A. (2001) MODELLER A Program for Protein Structure Modeling (available at http://guitar.rockefeller.edu/modeller/).
38. Sawaya, M.R., Krogmann, D.W., Serag, A., Ho, K.K., Yeates, T.O. and Kerfeld, C.A. (2001) Structures of cytochrome c-549 and cytochrome c-6 from the cyanobacterium Arthrospira maxima. Biochemistry 40: 9215-9225.
39. Sheldrick, G.M. and Schneider, T.R. (2001) In Direct Methods for Macromolecules Methods in Macromolecular Crystallography. Edited by Turk, D. and Johnson, L. pp. 72-81. D. IOS Press, Amsterdam.
40. Shen, J.-R. and Inoue, Y. (1993) Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12 kDa protein, in cyanobacterial photosystem II. Biochemistry 32: 1825-1832.
41. Shen, J.-R., Qian, M., Inoue, Y. and Burnap, R.L. (1998) Functional characterization of Synechocystis sp. PCC 6803 delta-psbU and delta-psbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37: 1551-1558.
42. Sugiura, M. and Inoue, Y. (1999) Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having his-tagged CP43. Plant Cell Physiol. 40: 1219-1231.
43. van Rensen, J.J.S., Xu, C. and Govindjee (1999) Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis. Physiol. Plant. 105: 585-592.
44. 3 by hydrogen. Evidence for heme-heme interactions. J. Am. Chem. Soc. 110: 6617-6623.
45. Vrettos, J.S., Reifler, M.J., Kievit, O., Lakshmi, K.V., de Paula, J.C. and Brudvig G.W. (2001) Factors that determine the unusually low reduction potential of cytochrome c-550 in cyanobacterial photosystem II. J. Biol. Inorg. Chem. 6: 708-716.
46. Walker, F.A. (1999) Magnetic spectroscopic (EPR, ESEEM, Mossbauer, MCD and NMR) studies of low-spin ferriheme centers and their corresponding heme proteins. Coord. Chem. Rev. 186: 471-534.
47. Walker, F.A., Reis, D. and Balke, V.L. (1984) Models of the cytochromes b. 5. EPR studies of low-spin iron(III) tetraphenylporphyrins. J. Am. Chem. Soc. 106: 6888-6898.
48. 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.