A heterogeneous tag-attachment to the homodimeric type 1 photosynthetic reaction center core protein in the green sulfur bacterium Chlorobaculum tepidum

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 7, 2011, Pages 803-812

  Azai, Chihiro ^a   Kim, Kwang ^a   Kondo, Toru ^b   Harada, Jiro ^c   Itoh, Shigeru ^b   Oh Oka, Hirozo ^a  

^a OSAKA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Electron paramagnetic resonance; Green sulfur bacteria; Histidine tag; Iron sulfur cluster; LC MS MS; Type 1 reaction center

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; HOMODIMER; NICKEL; POLYHISTIDINE TAG;

6XHIS TAG PSCA GENE; ABSORPTION; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; CELL ORGANELLE; CHEMICAL ANALYSIS; CHLOROBACULUM TEPIDUM; CHLOROBI; CHLOROSOME; ELECTRON SPIN RESONANCE; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE INACTIVATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; PHOTOSYNTHESIS; PRIORITY JOURNAL; PSCA GENE; PURIFICATION; RECA GENE; SITE DIRECTED MUTAGENESIS; TEMPERATURE MEASUREMENT;

BACTERIAL PROTEINS; CHLOROBI; ELECTRON SPIN RESONANCE SPECTROSCOPY; GENETIC ENGINEERING; MASS SPECTROMETRY; MUTAGENESIS, SITE-DIRECTED; PHENOTYPE; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM I PROTEIN COMPLEX; PROTEIN CONFORMATION; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; REC A RECOMBINASES; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); CHLOROBACULUM TEPIDUM; CHLOROBI;

EID: 79956103115     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.03.007     Document Type: Article

References (64)

1. J.T. Beatty, J. Overmann, M.T. Lince, A.K. Manske, A.S. Lang, R.E. Blankenship, C.L. Van Dover, T.A. Martinson, and F.G. Plumley An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent Proc. Natl. Acad. Sci. U.S.A. 102 2005 9306 9310 (Pubitemid 40923559)
2. J.M. Olson Chlorophyll organization and function in green photosynthetic bacteria Photochem. Photobiol. 67 1998 61 75 (Pubitemid 128471961)
3. C. Azai, Y. Tsukatani, J. Harada, and H. Oh-oka Sulfur oxidation in mutants of the photosynthetic green sulfur bacterium Chlorobium tepidum devoid of cytochrome c-554 and SoxB Photosynth. Res. 100 2009 57 65
4. N.U. Frigaard, and D.A. Bryant Genomic insight into the sulfur metabolism of phototropic green sulfur bacteria H. Rüdiger, Sulfur Metabolism in Phototrophic Organisms 2008 Springer New York 337 355
5. G. Hauska, T. Schoedl, H. Remigy, and G. Tsiotis The reaction center of green sulfur bacteria(1) Biochim. Biophys. Acta 1507 2001 260 277 (Pubitemid 33001524)
6. P. Jordan, P. Fromme, H.T. Witt, O. Klukas, W. Saenger, and N. Krauss Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution Nature 411 2001 909 917 (Pubitemid 32601481)
7. B. Jagannathan, and J.H. Golbeck Unifying principles in homodimeric type I photosynthetic reaction centers: properties of PscB and the FA FB and FX iron-sulfur clusters in green sulfur bacteria Biochim. Biophys. Acta 1777 2008 1535 1544
8. H. Oh-oka, S. Kamei, H. Matsubara, M. Iwaki, and S. Itoh Two molecules of cytochrome c function as the electron donors to P840 in the reaction center complex isolated from a green sulfur bacterium. Chlorobium tepidum FEBS Lett. 365 1995 30 34
9. H. Oh-oka, M. Iwaki, and S. Itoh Membrane-bound cytochrome cz couples quinol oxidoreductase to the P840 reaction center complex in isolated membranes of the green sulfur bacterium Chlorobium tepidum Biochemistry 37 1998 12293 12300 (Pubitemid 28411316)
10. Y. Tsukatani, C. Azai, T. Kondo, S. Itoh, and H. Oh-Oka Parallel electron donation pathways to cytochrome c(z) in the type I homodimeric photosynthetic reaction center complex of Chlorobium tepidum Biochim. Biophys. Acta 1777 2008 1211 1217
11. H. Oh-oka, M. Iwaki, and S. Itoh Viscosity dependence of the electron transfer rate from bound cytochrome c to P840 in the photosynthetic reaction center of the green sulfur bacterium Chlorobium tepidum Biochemistry 36 1997 9267 9272 (Pubitemid 27329513)
12. M. Higuchi, Y. Hirano, Y. Kimura, H. Oh-oka, K. Miki, and Z.Y. Wang Overexpression, characterization, and crystallization of the functional domain of cytochrome c(z) from Chlorobium tepidum Photosynth. Res. 102 2009 77 84
13. Y. Hirano, M. Higuchi, C. Azai, H. Oh-Oka, K. Miki, and Z.Y. Wang Crystal structure of the electron carrier domain of the reaction center cytochrome c(z) subunit from green photosynthetic bacterium Chlorobium tepidum J. Mol. Biol. 397 2010 1175 1187
14. J.M. Olson The FMO Protein Photosynth. Res. 80 2004 181 187 (Pubitemid 38889626)
15. R.E. Fenna, and B.W. Matthews Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola Nature 258 1975 573 577
16. D.E. Tronrud, J. Wen, L. Gay, and R.E. Blankenship The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria Photosynth. Res. 100 2009 79 87
17. Y. Tsukatani, R. Miyamoto, S. Itoh, and H. Oh-Oka Function of a PscD subunit in a homodimeric reaction center complex of the photosynthetic green sulfur bacterium Chlorobium tepidum studied by insertional gene inactivation. Regulation of energy transfer and ferredoxin-mediated NADP + reduction on the cytoplasmic side J. Biol. Chem. 279 2004 51122 51130 (Pubitemid 40017854)
18. P. Heathcote, M.R. Jones, and P.K. Fyfe Type I photosynthetic reaction centres: structure and function Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 231 243 (Pubitemid 36178232)
19. B. Kjaer, N.U. Frigaard, F. Yang, B. Zybailov, M. Miller, J.H. Golbeck, and H.V. Scheller Menaquinone-7 in the reaction center complex of the green sulfur bacterium Chlorobium vibrioforme functions as the electron acceptor A1 Biochemistry 37 1998 3237 3242 (Pubitemid 28125549)
20. N. Kusumoto, P. Setif, K. Brettel, D. Seo, and H. Sakurai Electron transfer kinetics in purified reaction centers from the green sulfur bacterium Chlorobium tepidum studied by multiple-flash excitation Biochemistry 38 1999 12124 12137
21. S. Takaichi, and H. Oh-oka Pigment composition in the reaction center complex from the thermophilic green sulfur bacterium. Chlorobium tepidum: carotenoid glucoside esters, menaquinone and chlorophylls Plant Cell Physiol. 40 1999 691 694 (Pubitemid 29360683)
22. A. van der Est, C. Hager-Braun, W. Leibl, G. Hauska, and D. Stehlik Transient electron paramagnetic resonance spectroscopy on green-sulfur bacteria and heliobacteria at two microwave frequencies Biochim. Biophys. Acta 1409 1998 87 98 (Pubitemid 28560221)
23. M. Iwaki, S. Itoh, S. Kamei, H. Matsubara, and H. Oh-oka Time-resolved spectroscopy of chlorophyll-a like electron acceptor in the reaction center complex of the green sulfur bacterium Chlorobium tepidum Plant Cell Physiol. 40 1999 1021 1028 (Pubitemid 29527031)
24. P. Heathcote, P.K. Fyfe, and M.R. Jones Reaction centres: the structure and evolution of biological solar power Trends Biochem. Sci. 27 2002 79 87 (Pubitemid 34164323)
25. H. Oh-oka Type 1 reaction center of photosynthetic heliobacteria Photochem. Photobiol. 83 2007 177 186 (Pubitemid 46697238)
26. R. Miyamoto, H. Mino, T. Kondo, S. Itoh, and H. Oh-Oka An electron spin-polarized signal of the P800 + A1(Q)- state in the homodimeric reaction center core complex of Heliobacterium modesticaldum Biochemistry 47 2008 4386 4393 (Pubitemid 351522087)
27. B.A. Diner, and F. Rappaport Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis Annu. Rev. Plant Biol. 53 2002 551 580 (Pubitemid 36257507)
28. M.C. Wakeham, and M.R. Jones Rewiring photosynthesis: engineering wrong-way electron transfer in the purple bacterial reaction centre Biochem. Soc. Trans. 33 2005 851 857 (Pubitemid 41160878)
29. A.N. Webber, and V.M. Ramesh Mutagenesis of Ligands to the Cofactors in Photosystem I J.H. Golbeck, Photosystem I: The Light-Driven Plastcyanin: Ferredoxin Oxidoreductase 2006 Springer 193 204
30. Y. Li, A. van der Est, M.G. Lucas, V.M. Ramesh, F. Gu, A. Petrenko, S. Lin, A.N. Webber, F. Rappaport, and K. Redding Directing electron transfer within Photosystem I by breaking H-bonds in the cofactor branches Proc. Natl. Acad. Sci. U.S.A. 103 2006 2144 2149 (Pubitemid 43271637)
31. S. Santabarbara, K. Reifschneider, A. Jasaitis, F. Gu, G. Agostini, D. Carbonera, F. Rappaport, and K.E. Redding Interquinone electron transfer in photosystem I as evidenced by altering the hydrogen bond strength to the phylloquinone(s) J. Phys. Chem. B 114 2010 9300 9312
32. N.U. Frigaard, and D.A. Bryant Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation Appl. Environ. Microbiol. 67 2001 2538 2544 (Pubitemid 33639724)
33. N.U. Frigaard, and D.A. Bryant Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria Arch. Microbiol. 182 2004 265 276 (Pubitemid 39403202)
34. J.A. Eisen, K.E. Nelson, I.T. Paulsen, J.F. Heidelberg, M. Wu, R.J. Dodson, R. Deboy, M.L. Gwinn, W.C. Nelson, D.H. Haft, E.K. Hickey, J.D. Peterson, A.S. Durkin, J.L. Kolonay, F. Yang, I. Holt, L.A. Umayam, T. Mason, M. Brenner, T.P. Shea, D. Parksey, W.C. Nierman, T.V. Feldblyum, C.L. Hansen, M.B. Craven, D. Radune, J. Vamathevan, H. Khouri, O. White, T.M. Gruber, K.A. Ketchum, J.C. Venter, H. Tettelin, D.A. Bryant, and C.M. Fraser The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium Proc. Natl. Acad. Sci. U.S.A. 99 2002 9509 9514 (Pubitemid 34764644)
35. E.C. Abresch, H.L. Axelrod, J.T. Beatty, J.A. Johnson, R. Nechushtai, and M.L. Paddock Characterization of a highly purified, fully active, crystallizable RC-LH1-PufX core complex from Rhodobacter sphaeroides Photosynth. Res. 86 2005 61 70 (Pubitemid 41361261)
36. T.M. Bricker, J. Morvant, N. Masri, H.M. Sutton, and L.K. Frankel Isolation of a highly active photosystem II preparation from Synechocystis 6803 using a histidine-tagged mutant of CP 47 Biochim. Biophys. Acta 1409 1998 50 57 (Pubitemid 28511112)
37. M. Cullen, N. Ray, S. Husain, J. Nugent, J. Nield, and S. Purton A highly active histidine-tagged Chlamydomonas reinhardtii Photosystem II preparation for structural and biophysical analysis Photochem. Photobiol. Sci. 6 2007 1177 1183 (Pubitemid 350045987)
38. H. Fey, D. Piano, R. Horn, D. Fischer, M. Schmidt, S. Ruf, W.P. Schroder, R. Bock, and C. Buchel Isolation of highly active photosystem II core complexes with a His-tagged Cyt b559 subunit from transplastomic tobacco plants Biochim. Biophys. Acta 1777 2008 1501 1509
39. J.O. Goldsmith, and S.G. Boxer Rapid isolation of bacterial photosynthetic reaction centers with an engineered poly-histidine tag Biochim. Biophys. Acta 1276 1996 171 175 (Pubitemid 26321078)
40. G. Gulis, K.V. Narasimhulu, L.N. Fox, and K.E. Redding Purification of His6-tagged Photosystem I from Chlamydomonas reinhardtii Photosynth. Res. 96 2008 51 60
41. H. Kubota, I. Sakurai, K. Katayama, N. Mizusawa, S. Ohashi, M. Kobayashi, P. Zhang, E.M. Aro, and H. Wada Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits Biochim. Biophys. Acta 1797 2010 98 105
42. M. Sugiura, Y. Inoue, and J. Minagawa Rapid and discrete isolation of oxygen-evolving His-tagged photosystem II core complex from Chlamydomonas reinhardtii by Ni2+ affinity column chromatography FEBS Lett. 426 1998 140 144 (Pubitemid 28198172)
43. M. Sugiura, F. Rappaport, K. Brettel, T. Noguchi, A.W. Rutherford, and A. Boussac Site-directed mutagenesis of Thermosynechococcus elongatus photosystem II: the O2-evolving enzyme lacking the redox-active tyrosine D Biochemistry 43 2004 13549 13563 (Pubitemid 39391156)
44. H. Tang, and P.R. Chitnis Addition of C-terminal histidyl tags to PsaL and PsaK1 proteins of cyanobacterial photosystem I Indian J. Biochem. Biophys. 37 2000 433 440
45. S.C. Kowalczykowski, D.A. Dixon, A.K. Eggleston, S.D. Lauder, and W.M. Rehrauer Biochemistry of homologous recombination in Escherichia coli Microbiol. Rev. 58 1994 401 465
46. T.M. Wahlund, and M.T. Madigan Genetic transfer by conjugation in the thermophilic green sulfur bacterium Chlorobium tepidum J. Bacteriol. 177 1995 2583 2588
47. H.D. Schweizer Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis Biotechniques 15 1993 831 834
48. P. Prentki, and H.M. Krisch In vitro insertional mutagenesis with a selectable DNA fragment Gene 29 1984 303 313 (Pubitemid 14038235)
49. N.U. Frigaard, Y. Sakuragi, and D.A. Bryant Gene inactivation in the cyanobacterium Synechococcus sp. PCC 7002 and the green sulfur bacterium Chlorobium tepidum using in vitro-made DNA constructs and natural transformation Methods Mol. Biol. 274 2004 325 340
50. J.A. Maresca, A. Gomez Maqueo Chew, M.R. Ponsati, N.U. Frigaard, J.G. Ormerod, and D.A. Bryant The bchU gene of Chlorobium tepidum encodes the c-20 methyltransferase in bacteriochlorophyll c biosynthesis J. Bacteriol. 186 2004 2558 2566 (Pubitemid 38525908)
51. H. Oh-oka, S. Kakutani, H. Matsubara, R. Malkin, and S. Itoh Isolation of the photoactive reaction center complex that contains three types of Fe-S centers and a cytochrome c subunit from the green sulfur bacterium Chlorobium limicola f. thiosulfatophilum, strain Larsen Plant Cell Physiol. 34 1993 93 101
52. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
53. I. Erill, S. Campoy, and J. Barbe Aeons of distress: an evolutionary perspective on the bacterial SOS response FEMS Microbiol. Rev. 31 2007 637 656 (Pubitemid 47621761)
54. J.M. Olson, K.D. Philipson, and K. Sauer Circular dichroism and absorption spectra of bacteriochlorophyll-protein and reaction center complexes from Chlorobium thiosulfatophilum Biochim. Biophys. Acta 292 1973 206 217
55. T.E. Meyer, R.G. Bartsch, M.A. Cusanovich, and J.H. Mathewson The cytochromes of Chlorobium thiosulfatophilum Biochim. Biophys. Acta 153 1968 854 861
56. C. Francke, H.P. Permentier, E.M. Franken, S. Neerken, and J. Amesz Isolation and properties of photochemically active reaction center complexes from the green sulfur bacterium Prosthecochloris aestuarii Biochemistry 36 1997 14167 14172 (Pubitemid 27509852)
57. U. Feiler, W. Nitschke, and H. Michel Characterization of an improved reaction center preparation from the photosynthetic green sulfur bacterium Chlorobium containing the FeS centers FA and FB and a bound cytochrome subunit Biochemistry 31 1992 2608 2614
58. W. Nitschke, U. Feiler, and A.W. Rutherford Photosynthetic reaction center of green sulfur bacteria studied by EPR Biochemistry 29 1990 3834 3842 (Pubitemid 20151292)
59. I.R. Vassiliev, M.T. Ronan, G. Hauska, and J.H. Golbeck The bound electron acceptors in green sulfur bacteria: resolution of the g-tensor for the F(X) iron-sulfur cluster in Chlorobium tepidum Biophys. J. 78 2000 3160 3169 (Pubitemid 30396944)
60. A.J. Clark, and A.D. Margulis Isolation and characterization of recombination-deficient strains of Escherichia coli K-12 Proc. Natl. Acad. Sci. U.S.A. 53 1965 451 459
61. I.P. Chen, and H. Michel Cloning, sequencing, and characterization of the recA gene from Rhodopseudomonas viridis and construction of a recA strain J. Bacteriol. 180 1998 3227 3232 (Pubitemid 28285040)
62. R. Minda, J. Ramchandani, V.P. Joshi, and S.K. Bhattacharjee A homozygous recA mutant of Synechocystis PCC6803: construction strategy and characteristics eliciting a novel RecA independent UVC resistance in dark Mol. Genet. Genomics 274 2005 616 624 (Pubitemid 41746828)
63. H. Li, S. Jubelirer, A.M. Garcia Costas, N.U. Frigaard, and D.A. Bryant Multiple antioxidant proteins protect Chlorobaculum tepidum against oxygen and reactive oxygen species Arch. Microbiol. 191 2009 853 867
64. A. Skerra, and T.G. Schmidt Applications of a peptide ligand for streptavidin: the Strep-tag Biomol. Eng. 16 1999 79 86 (Pubitemid 30184842)