Crystal structure at 1.5 Å resolution of the PsbV2 cytochrome from the cyanobacterium Thermosynechococcus elongatus

FEBS Letters

Volumn 587, Issue 19, 2013, Pages 3267-3272

  Suga, Michihiro ^a   Lai, Thanh Lan ^b   Sugiura, Miwa ^c,d   Shen, Jian Ren ^a   Boussac, Alain ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b CEA SACLAY   (France)

^c EHIME UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Crystal structure; Cyanobacteria; Cytochrome c; His Cys coordination; PsbV2

Indexed keywords

CYTOCHROME C; DIMER; HEME; PSBV2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; PRIORITY JOURNAL; STRUCTURE ANALYSIS; THERMOSYNECHOCOCCUS ELONGATUS;

CRYSTAL STRUCTURE; CYANOBACTERIA; CYTOCHROME C; HIS/CYS COORDINATION; PSBV2;

CRYSTALLIZATION; CYANOBACTERIA; CYTOCHROMES; DIMERIZATION; MODELS, MOLECULAR; PROTEIN CONFORMATION;

CYANOBACTERIA; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 84884286166     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.08.023     Document Type: Article

References (46)

1. Y. Nakamura, T. Kaneko, S. Sato, M. Ikeuchi, H. Katoh, S. Sasamoto, A. Watanabe, M. Iriguchi, K. Kawashima, T. Kimura, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, N. Nakazaki, S. Shimpo, M. Sugimoto, M. Takeuchi, M. Yamada, and S. Tabata Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 DNA Res. 9 2002 123 130
2. M. Sugiura, and Y. Inoue Highly purified thermo-stable oxygen evolving Photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43 Plant Cell Physiol. 40 1999 1219 1231
3. 2 evolving enzyme lacking the redox active tyrosine D Biochemistry 43 2004 13549 13563
4. 680, of Photosystem II in Thermosynechococcus elongatus Biochim. Biophys. Acta 1777 2008 331 342
5. S. Ogami, A. Boussac, and M. Sugiura Deactivation processes in PsbA1-photosystem II and PsbA3-photosystem II under photoinhibitory conditions in the cyanobacterium Thermosynechococcus elongatus Biochim. Biophys. Acta 1817 2012 1322 1330
6. Z in Photosystem II from Thermosynechococcus elongatus in which PsbA2 is the D1 protein J. Biol. Chem. 287 2012 13336 13347
7. K. Takasaka, M. Iwai, Y. Umena, K. Kawakami, Y. Ohmori, M. Ikeuchi, Y. Takahashi, N. Kamiya, and J.-R. Shen Structural and functional studies on Ycf12 (Psb30) and PsbZ-deletion mutants from a thermophilic cyanobacterium Biochim. Biophys. Acta 1797 2010 278 284
8. M.M. Nowaczyk, K. Krause, M. Mieseler, A. Sczibilanski, M. Ikeuchi, and M. Rogner Deletion of psbJ leads to accumulation of Psb27-Psb28 photosystem II complexes in Thermosynechococcus elongatus Biochim. Biophys. Acta 1817 2010 1339 1345
9. M. Iwai, H. Katoh, M. Katayama, and M. Ikeuchi Improved genetic transformation of the thermophilic cyanobacterium, Thermosynechococcus elongatus BP-1 Plant Cell Physiol. 45 2004 171 175
10. A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, and W. Saenger Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels, and chloride Nat. Struct. Mol. Biol. 16 2009 334 342
11. P. Jordan, P. Fromme, H.T. Witt, O. Klukas, W. Saenger, and N. Krauss Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution Nature 411 2001 909 917
12. K.N. Ferreira, T.M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata Architecture of the photosynthetic oxygen-evolving center Science 303 2004 1831 1838
13. A. Zouni, H.T. Witt, J. Kern, P. Fromme, N. Krauss, W. Saenger, and P. Orth Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution Nature 409 2001 739 743
14. Y. Umena, K. Kawakami, J.-R. Shen, and N. Kamiya Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Nature 473 2011 55 60
15. C.A. Kerfeld, and D.W. Krogmann Photosynthetic cytochromes c in cyanobacteria, algae, and plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 1998 397 425
16. J.-R. Shen, M. Ikeuchi, and Y. Inoue Stoichiometric association of extrinsic cytochrome c-550 and 12 kDa protein with a highly purified oxygen-evolving photosystem II core complex from Synechococcus vulcanus FEBS Lett. 301 1992 145 149
17. J.-R. Shen, and Y. Inoue Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12 kDa protein, in cyanobacterial photosystem II Biochemistry 32 1993 1825 1832
18. C.A. Kerfeld, M.R. Sawaya, H. Bottin, K.T. Tran, M. Sugiura, D. Cascio, A. Desbois, T.O. Yeates, D. Kirilovsky, and A. Boussac Structural and EPR characterization of the soluble form of cytochrome c-550 and of the psbV2 gene product from the cyanobacterium Thermosynechococcus elongatus Plant Cell Physiol. 44 2003 697 706
19. J.-R. Shen, and Y. Inoue Cellular localization of cytochrome c-550. Its specific association with cyanobacterial photosystem II J. Biol. Chem. 268 1993 20408 20413
20. I. Enami, S. Yoshihara, A. Tohri, A. Okumura, H. Ohta, and J.-R. Shen Cross-reconstitution of various extrinsic proteins and photosystem II complexes from cyanobacteria, red algae and higher plants Plant Cell Physiol. 41 2000 1354 1364
21. J.-R. Shen, M. Qian, Y. Inoue, and R.L. Burnap Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial PSII Biochemistry 37 1998 1551 1558
22. M.R. Sawaya, D.W. Krogmann, A. Serag, K.K. Ho, T.O. Yeates, and C.A. Kerfeld Structures of cytochrome c-549 and cytochrome c(6) from the cyanobacterium Arthrospira Biochemistry 40 2001 9215 9225
23. M. Beissinger, H. Sticht, M. Sutter, A. Ejchart, W. Haehnel, and P. Rosch Solution structure of cytochrome c(6) from the thermophilic cyanobacterium Synechococcus elongatus EMBO J. 17 1998 27 36
24. M. Roncel, D. Kirilovsky, F. Guerrero, A. Serrano, and J.-M. Ortega Photosynthetic cytochrome c550 Biochim. Biophys. Acta 1817 2012 1152 1163
25. M.P. Malakhov, H. Wada, D.A. Los, V.E. Semenenko, and N. Murata A new type of cytochrome-C from Synechocystis 6803 J. Plant Physiol. 144 1994 259 264
26. 6 and plastocyanine from the cyanobacterium Synechocystis sp. PCC 6803 FEBS Lett. 517 2002 50 54
27. A. Boussac, K. Koyama, and M. Sugiura The Tll0287 protein is a hemoprotein associated with the PsbA2-photosystem II complex in Thermosynechococcus elongatus Biochim. Biophys. Acta 2013 10.1016/j.bbabio.2013. 06.002 in press
28. H. Katoh, S. Itoh, J.-R. Shen, and M. Ikeuchi 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 2001 599 607
29. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
30. Collaborative Computational Project, number 4. The CCP4 Suite: Programs for Protein Crystallography. (1994) Acta Crystallogr. D 50, 760-763.
31. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D 60 2004 2126 2132
32. P.D. Adams PHENIX: a comprehensive python-based system for macromolecular structure solution Acta Crystallogr. D 66 2010 213 221
33. V. Chen, W. Arendall III, J. Headd, D. Keedy, R. Immormino, G. Kapral, L. Murray, J. Richardson, and D. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D 66 2010 12 21
34. J. Padilla, and T. Yeates A statistic for local intensity differences: robustness to anisotropy and pseudo-centering and utility for detecting twinning Acta Crystallogr. D 59 2003 1124 1130
35. F. Grein, S.S. Venceslau, L. Schneider, P. Hildebrandt, S. Todorovic, I.A.C. Pereira, and C. Dahl DsrJ, an essential part of the DsrMKJOP transmembrane complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual trihem cytochrome c Biochemistry 49 2010 8920 8929
36. K. Denkmann, F. Grein, R. Zigann, A. Siemen, J. Bergmann, S. van Helmont, A. Nicolai, I.C.A. Pereira, and C. Dahl Thiosulfate deshydrogenase: a widespread unusual acidophilic c-type cytochrome Envir. Microbiol. 14 2012 2673 2688
37. U. Kappler, and M.J. Maher The bacterial SoxAX cytochromes Cell. Mol. Life Sci. 70 2013 977 993
38. J. Alric, Y. Tsukatani, M. Yoshida, K. Matsuura, K. Shimada, R. Hienerwadel, B. Shoepp-Cothenet, W. Nitschke, K.V.P. Nagashima, and A. Verméglio Structural and functional characterization of the unusual triheme cytochrome bound to the reaction center of Rhodovulum sulfidophilum J. Biol. Chem. 279 2004 26090 26097
39. G. Vandriessche, B. Devreese, J.C. Fitch, T.E. Meyer, M.A. Cusanovich, and J.J.V. VanBeeumen GHP, a new c-type green heme protein from Halobacterium salexigens and other proteobacteria FEBS J. 273 2006 2801 2811
40. S. Ukita, T. Fujii, D. Hira, T. Nishiyama, T. Kawase, C.T. Migita, and K.A. Furukawa Heterodimeric cytochrome c complex with a very low redox potential from an anaerobic ammonium-oxidizing enrichment culture FEMS Microbiol. Lett. 313 2010 61 67
41. M. Meier, M. Janosik, V. Kery, J.P. Kraus, and P. Burkhard Structure of human cystathionine-synthase: a unique pyridoxal 5′-phosphate-dependent heme protein EMBO J. 20 2001 3910 3916
42. S. Pazicni, M.M. Cherney, G.S. Lukat-Rodgers, J. Oliveriusová, K.R. Rodgers, J.P. Kraus, and J.N. Burstyn The heme of cystathionine-synthase likely undergoes a thermally induced redox-mediated ligand switch Biochemistry 44 2005 16785 16795
43. A.L. Raphael, and H.B. Gray Semi-synthesis of axial ligand (position 80) mutants of cytochrome c J. Am. Chem. Soc. 113 1991 1038 1040
44. J. Peisach, W.E. Blumberg, and A. Adler Electron paramagnetic resonance studies of iron porphyrin and chlorin systems Ann. N.Y. Acad. Sci. 206 1973 310 327
45. F.A. Walker Magnetic spectroscopic (EPR, ESEEM, Mossbauer, MCD and NMR) studies of low-spin ferriheme centers and their corresponding heme proteins Coord. Chem. Rev. 186 1999 471 534
46. D. Kirilovsky, M. Roncel, A. Boussac, A. Wilson, J.-L. Zurita, J.-M. Ducruet, H. Bottin, M. Sugiura, J.-M. Ortega, and A.W. Rutherford Cytochrome c550 in the cyanobacterium Thermosynechococcus elongatus: study of redox mutants J. Biol. Chem. 279 2004 52869 52880