Multiple Rieske proteins in prokaryotes: Where and why?

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1710, Issue 1, 2005, Pages 1-12

  Schneider, Dirk ^a   Schmidt, Christian L ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Cyanobacteria; Cytochrome b6f; Cytochrome bc1; Gene family; Sulfolobus

Indexed keywords

IRON SULFUR PROTEIN; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; AQUIFEX AEOLICUS; CYANOBACTERIUM; DEINOCOCCUS RADIODURANS; ELECTRON TRANSPORT; EUKARYOTE; GENE EXPRESSION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; RHODOPSEUDOMONAS PALUSTRIS; THERMUS THERMOPHILUS;

ANIMALS; ARCHAEAL PROTEINS; BACTERIAL PROTEINS; ELECTRON TRANSPORT COMPLEX III; IRON-SULFUR PROTEINS; PHYLOGENY; PROKARYOTIC CELLS;

AQUIFEX AEOLICUS; CYANOBACTERIA; DEINOCOCCUS RADIODURANS; EUKARYOTA; PROKARYOTA; RHODOPSEUDOMONAS PALUSTRIS; SULFOLOBUS; THERMUS THERMOPHILUS;

EID: 27644586323     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2005.09.003     Document Type: Review

References (81)

1. J.S. Rieske, R.E. Hansen, and W.S. Zaugg Studies on the electron transfer system J. Biol. Chem. 239 1964 3017 3030
2. C.L. Schmidt, and L. Shaw A comprehensive phylogenetic analysis of Rieske and Rieske-type iron-sulfur proteins J. Bioenerg. Biomembr. 33 2001 9 26
3. T.A. Link, W.R. Hagen, A.J. Pierik, C. Assmann, and G. von Jagow Determination of the redox properties of the Rieske [2Fe-2S] cluster of bovine heart bc1 complex by direct electrochemistry of a water-soluble fragment Eur. J. Biochem. 208 1992 685 691
4. D. Kuila, and J.A. Fee Evidence for a redox-linked ionizable group associated with the [2Fe-2S] cluster of Thermus Rieske protein J. Biol. Chem. 261 1986 2768 2771
5. Y. Zu, M.M. Couture, D.R. Kolling, A.R. Crofts, L.D. Eltis, J.A. Fee, and J. Hirst Reduction potentials of Rieske clusters: importance of the coupling between oxidation state and histidine protonation state Biochemistry 42 2003 12400 12408
6. C.L. Schmidt Rieske iron-sulfur proteins from extremophilic organisms J. Bioenerg. Biomembr. 36 2004 107 113
7. P.J. Ellis, T. Conrads, R. Hille, and P. Kuhn Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 A and 2.03 A Structure (Camb.) 9 2001 125 132
8. E. Lebrun, M. Brugna, F. Baymann, D. Muller, D. Lievremont, M.C. Lett, and W. Nitschke Arsenite oxidase, an ancient bioenergetic enzyme Mol. Biol. Evol. 20 2003 686 693
9. G.L. Anderson, J. Williams, and R. Hille The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase J. Biol. Chem. 267 1992 23674 23682
10. G. Van Driessche, I. Vandenberghe, B. Devreese, B. Samyn, T.E. Meyer, R. Leigh, M.A. Cusanovich, R.G. Bartsch, U. Fischer, and J.J. Van Beeumen Amino acid sequences and distribution of high-potential iron-sulfur proteins that donate electrons to the photosynthetic reaction center in phototropic proteobacteria J. Mol. Evol. 57 2003 181 199
11. E.A. Berry, M. Guergova-Kuras, L.S. Huang, and A.R. Crofts Structure and function of cytochrome bc complexes Annu. Rev. Biochem. 69 2000 1005 1075
12. S. Iwata, M. Saynovits, T.A. Link, and H. Michel Structure of a water soluble fragment of the 'Rieske' iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5 A resolution Structure 4 1996 567 579
13. T. Merbitz-Zahradnik, K. Zwicker, J.H. Nett, T.A. Link, and B.L. Trumpower Elimination of the disulfide bridge in the Rieske iron-sulfur protein allows assembly of the [2Fe-2S] cluster into the Rieske protein but damages the ubiquinol oxidation site in the cytochrome bc1 complex Biochemistry 42 2003 13637 13645
14. Y. Zu, J.A. Fee, and J. Hirst Breaking and re-forming the disulfide bond at the high-potential, respiratory-type Rieske [2Fe-2S] center of thermus thermophilus: characterization of the sulfhydryl state by protein-film voltammetry Biochemistry 41 2002 14054 14065
15. T. Schroter, O.M. Hatzfeld, S. Gemeinhardt, M. Korn, T. Friedrich, B. Ludwig, and T.A. Link Mutational analysis of residues forming hydrogen bonds in the Rieske [2Fe-2S] cluster of the cytochrome bc1 complex in Paracoccus denitrificans Eur. J. Biochem. 255 1998 100 106
16. E. Denke, T. Merbitz-Zahradnik, O.M. Hatzfeld, C.H. Snyder, T.A. Link, and B.L. Trumpower Alteration of the midpoint potential and catalytic activity of the Rieske iron-sulfur protein by changes of amino acids forming hydrogen bonds to the iron-sulfur cluster J. Biol. Chem. 273 1998 9085 9093
17. L.M. Hunsicker-Wang, A. Heine, Y. Chen, E.P. Luna, T. Todaro, Y.M. Zhang, P.A. Williams, D.E. McRee, J. Hirst, C.D. Stout, and J.A. Fee High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison Biochemistry 42 2003 7303 7317
18. M. Brugna, W. Nitschke, M. Asso, B. Guigliarelli, D. Lemesle-Meunier, and C. Schmidt Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes: II. The Rieske protein of phylogenetically distant acidophilic organisms J. Biol. Chem. 274 1999 16766 16772
19. A. Kröger, and G. Unden G. Lenaz Coenzyme Q: The Function of Menaquinone in Bacterial Electron Transport 1985 John Wiley and Sons Chichester 256 285
20. S. de Vries, J.A. Berden, and E.C. Slater B.L. Trumpower Function of Quinones in Energy Conserving Systems 1985 Academic Press New York 235 246
21. A.V. Vener, P.J. van Kan, P.R. Rich, I.I. Ohad, and B. Andersson Plastoquinol at the quinol oxidation site of r educed cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash Proc. Natl. Acad. Sci. U. S. A. 94 1997 1585 1590
22. G. Schafer, M. Engelhard, and V. Muller Bioenergetics of the Archaea Microbiol. Mol. Biol. Rev. 63 1999 570 620
23. T.A. Link, O.M. Hatzfeld, P. Unalkat, J.K. Shergill, R. Cammack, and J.R. Mason Comparison of the "Rieske" [2Fe-2S] center in the bc1 complex and in bacterial dioxygenases by circular dichroism spectroscopy and cyclic voltammetry Biochemistry 35 1996 7546 7552
24. R.J. Lewis, R.C. Prince, P.L. Dutton, D.B. Knaff, and T.A. Krulwich The respiratory chain of Bacillus alcalophilus and its nonalkalophilic mutant derivative J. Biol. Chem. 256 1981 10543 10549
25. J.S. Knight, C.M. Duckett, J.A. Sullivan, A.R. Walker, and J.C. Gray Tissue-specific, light-regulated and plastid-regulated expression of the single-copy nuclear gene encoding the chloroplast Rieske FeS protein of Arabidopsis thaliana Plant Cell Physiol. 43 2002 522 531
26. F. Madueno, J.A. Napier, F.J. Cejudo, and J.C. Gray Import and processing of the precursor of the Rieske FeS protein of tobacco chloroplasts Plant Mol. Biol. 20 1992 289 299
27. J. Steppuhn, C. Rother, J. Hermans, T. Jansen, J. Salnikow, G. Hauska, and R.G. Herrmann The complete amino-acid sequence of the Rieske FeS-precursor protein from spinach chloroplasts deduced from cDNA analysis Mol. Gen. Genet. 210 1987 171 177
28. A.H. Salter, B.J. Newman, J.A. Napier, and J.C. Gray Import of the precursor of the chloroplast Rieske iron-sulphur protein by pea chloroplasts Plant Mol. Biol. 20 1992 569 574
29. J. Huang, S. Friedhelm, D.F. Matzinger, and C.S. Levings III Flower-enhanced expression of a nuclear-encoded mitochondrial respiratory protein is associated with changes in mitochondrion number Plant Cell 6 1994 439 448
30. J.T. Huang, F. Struck, D.F. Matzinger, and C.S. Levings III Functional analysis in yeast of cDNA coding for the mitochondrial Rieske iron-sulfur protein of higher plants Proc. Natl. Acad. Sci. U. S. A. 88 1991 10716 10720
31. G. Brasseur, P. Bruscella, V. Bonnefoy, and D. Lemesle-Meunier The bc(1) complex of the iron-grown acidophilic chemolithotrophic bacterium Acidithiobacillus ferrooxidans functions in the reverse but not in the forward direction. Is there a second bc(1) complex? Biochim. Biophys. Acta 1555 2002 37 43
32. A. Elbehti, W. Nitschke, P. Tron, C. Michel, and D. Lemesle-Meunier Redox components of cytochrome bc-type enzymes in acidophilic prokar yotes: I. Characterization of the cytochrome bc1-type complex of the acidophilic ferrousion-oxidizing bacterium Thiobacillus ferrooxidans J. Biol. Chem. 274 1999 16760 16765
33. A. Elbehti, G. Brasseur, and D. Lemesle-Meunier First evidence for existence of an uphill electron transfer through the bc(1) and NADH-Q oxidoreductase complexes of the acidophilic obligate chemolithotrophic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans J. Bacteriol. 182 2000 3602 3606
34. G. Brasseur, G. Levican, V. Bonnefoy, D. Holmes, E. Jedlicki, and D. Lemesle-Meunier Apparent redundancy of electron transfer pathways via bc(1) complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans Biochim. Biophys. Acta 1656 2004 114 126
35. E. Maklashina, D.A. Berthold, and G. Cecchini Anaerobic expression of Escherichia coli succinate dehydrogenase: functional replacement of fumarate reductase in the respiratory chain during anaerobic growth J. Bacteriol. 180 1998 5989 5996
36. 1 complex of Rhodobacter sphaeroides blocking or impairing quinol oxidation Biochemistry 32 1993 8083 8091
37. 1 complex are essential for protein structure, properties of the [2Fe-2S] cluster, and communication with the quinone pool Biochemistry 36 1997 11675 11684
38. S. Ouchane, W. Nitschke, P. Bianco, A. Vermeglio, and C. Astier Multiple Rieske genes in prokaryotes: exchangeable Rieske subunits in the cytochrome bc-complex of Rubrivivax gelatinosus Mol. Microbiol. 57 2005 261 275
39. G. Deckert, P.V. Warren, T. Gaasterland, W.G. Young, A.L. Lenox, D.E. Graham, R. Overbeek, M.A. Snead, M. Keller, M. Aujay, R. Huber, R.A. Feldman, J.M. Short, G.J. Olsen, and R.V. Swanson The complete genome of the hyperthermophilic bacterium Aquifex aeolicus Nature 392 1998 353 358
40. 1 complex of the hyperthermophilic knallgasbacterium Aquifex aeolicus: properties and phylogenetic relationships Biochemistry 42 2003 10800 10808
41. W.R. Hagen, P.J. Silva, M.A. Amorim, P.L. Hagedoorn, H. Wassink, H. Haaker, and F.T. Robb Novel structure and redox chemistry of the prosthetic groups of the iron-sulfur flavoprotein sulfide dehydrogenase from Pyrococcus furiosus; evidence for a [2Fe-2S] cluster with Asp(Cys)3 ligands J. Biol. Inorg. Chem. 5 2000 527 534
42. J. Yu, L. Hederstedt, and P.J. Piggot The cytochrome bc complex (menaquinone:cytochrome c reductase) in Bacillus subtilis has a nontraditional subunit organization J. Bacteriol. 177 1995 6751 6760
43. D. Mooser, O. Maneg, C. Corvey, T. Steiner, F. Malatesta, M. Karas, T. Soulimane, and B. Ludwig A four-subunit cytochrome bc(1) complex complements the respiratory chain of Thermus thermophilus Biochim. Biophys. Acta 1708 2005 262 274
44. Y. Nakamura, T. Kaneko, S. Sato, M. Mimuro, H. Miyashita, T. Tsuchiya, S. Sasamoto, A. Watanabe, K. Kawashima, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, N. Nakazaki, S. Shimpo, C. Takeuchi, M. Yamada, and S. Tabata Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids (supplement) DNA Res. 10 2003 181 201
45. D. Schneider, U. Altenfeld, H. Thomas, S. Schrader, U. Muhlenhoff, and M. Rögner Sequence of the two operons encoding the four core subunits of the cytochrome b(6)f complex from the thermophilic cyanobacterium Synechococcus elongatus Biochim. Biophys. Acta 1491 2000 364 368
46. 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, C. Takeuchi, M. Yamada, and S. Tabata Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 (supplement) DNA Res. 9 2002 135 148
47. T. Kallas, S. Spiller, and R. Malkin Characterization of two operons encoding the cytochrome b6-f complex of the cyanobacterium Nostoc PCC 7906. Highly conserved sequences but different gene organization than in chloroplasts J. Biol. Chem. 263 1988 14334 14342
48. T. Kallas, S. Spiller, and R. Malkin Primary structure of cotranscribed genes encoding the Rieske Fe-S and cytochrome f proteins of the cyanobacterium Nostoc PCC 7906 Proc. Natl. Acad. Sci. U. S. A. 85 1988 5794 5798
49. 6f complex of Synechocystis PCC6803? J. Biol. Chem. 277 2002 10949 10954
50. S. Ehira, M. Ohmori, and N. Sato Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 DNA Res. 10 2003 97 113
51. 6f complex to structure changes in the Hinge region of the Rieske iron-sulfur protein J. Biol. Chem. 278 2003 20925 20933
52. 6f complex of Synechocystis sp. PCC 6803 J. Biol. Chem. 279 2004 39383 39388
53. D. Bordo, and P. Bork The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations EMBO Rep. 3 2002 741 746
54. S. Pagani, F. Bonomi, and P. Cerletti Enzymic synthesis of the iron-sulfur cluster of spinach ferredoxin Eur. J. Biochem. 142 1984 361 366
55. A.G. Murzin How far divergent evolution goes in proteins Curr. Opin. Struct. Biol. 8 1998 380 387
56. C.J. Carrell, H. Zhang, W.A. Cramer, and J.L. Smith Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein Structure 5 1997 1613 1625
57. L.M. Hunsicker-Wang, A. Heine, Y. Chen, E.P. Luna, T. Todaro, Y.M. Zhang, P.A. Williams, D.E. McRee, J. Hirst, C.D. Stout, and J.A. Fee High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison Biochemistry 42 2003 7303 7317
58. A. Kapazoglou, R.M. Mould, and J.C. Gray Assembly of the Rieske iron-sulphur protein into the cytochrome bf complex in thylakoid membranes of isolated pea chloroplasts Eur. J. Biochem. 267 2000 352 360
59. D. Stroebel, Y. Choquet, J.L. Popot, and D. Picot An atypical haem in the cytochrome b(6)f complex Nature 426 2003 413 418
60. 6f complex of oxygenic photosynthesis: tuning the cavity Science 302 2003 1009 1014
61. G. Brasseur, V. Sled, U. Liebl, T. Ohnishi, and F. Daldal The amino-terminal portion of the Rieske iron-sulfur protein contributes to the ubihydroquinone oxidation site catalysis of the Rhodobacter capsulatus bc1 complex Biochemistry 36 1997 11685 11696
62. M. Arnold, G. Hauska, and I. Maldener A special isoform of the Rieske-FeS protein is involved in heterocyst function of the cyanobacterium Anabaena sp PCC 7120 2004
63. U. Liebl, S. Pezennec, A. Riedel, E. Kellner, and W. Nitschke The Rieske FeS center from the gram-positive bacterium PS3 and its interaction with the menaquinone pool studied by EPR J. Biol. Chem. 267 1992 14068 14072
64. T.W. Johnson, G. Shen, B. Zybailov, D. Kolling, R. Reategui, S. Beauparlant, I.R. Vassiliev, D.A. Bryant, A.D. Jones, J.H. Golbeck, and P.R. Chitnis Recruitment of a foreign quinone into the A(1) site of photosystem I: I. Genetic and physiological characterization of phylloquinone biosynthetic pathway mutants in Synechocystis sp. pcc 6803 J. Biol. Chem. 275 2000 8523 8530
65. Y. Takahashi, K. Hirota, and S. Katho Multiple forms of P700-chlorophyll a-protein complexes from Synechococcus sp-The iron, quinone and carotenoid contents Photosynth. Res. 6 1985 183 192
66. G.P. Palace, J.E. Franke, and J.T. Warden Is phylloquinone an obligate electron carrier in photosystem I? FEBS Lett. 215 1987 58 62
67. J. Biggins, and P. Mathis Functional role of vitamin K in photosystem I of the cyanobacterium Synechocystis 6803 Biochemistry 27 1988 1494 1500
68. R. Malkin On the function of two vitamin K1 molecules in the PS I electron acceptor complex FEBS Lett. 208 1986 343 346
69. H.-U. Schoeder, and W. Lockau Phylloquinone copurifies with the large subunit of photosystem I FEBS Lett. 199 1986 23 27
70. P. Jordan, P. Fromme, H.T. Witt, O. Klukas, W. Saenger, N. Krausz, Three-dimensional structure of cyanobacterial photosystem I at 2.5[thinsp][angst] resolution. 411 (2001) 909-917.
71. G. Schmetterer D.A. Bryant The Molecular Biology of Cyanobacteria 1994 Kluwer Academic Publishers Dordrecht, Netherlands 409 435
72. 1-analogous complex in the respiratory chain of the hyperthermoacidophilic crenarchaeon Sulfolobus acidocaldarius J. Bioenerg. Biomembr. 35 2003 121 131
73. L. Komorowski, W. Verheyen, and G. Schafer The archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinole and cytochrome c oxidases Biol. Chem. 383 2002 1791 1799
74. C.L. Schmidt, S. Anemuller, and G. Schafer Two different respiratory Rieske proteins are expressed in the extreme thermoacidophilic crenarchaeon Sulfolobus acidocaldarius: cloning and sequencing of their genes FEBS Lett. 388 1996 43 46
75. M. Lubben, S. Arnaud, J. Castresana, A. Warne, S.P. Albracht, and M. Saraste A second terminal oxidase in Sulfolobus acidocaldarius Eur. J. Biochem. 224 1994 151 159
76. H. Bonisch, C.L. Schmidt, G. Schafer, and R. Ladenstein The structure of the soluble domain of an archaeal Rieske iron-sulfur protein at 1.1 A resolution J. Mol. Biol. 319 2002 791 805
77. T. Iwasaki, Y. Isogai, T. Iizuka, and T. Oshima Sulredoxin: a novel iron-sulfur protein of the thermoacidophilic archaeon Sulfolobus sp. strain 7 with a Rieske-type [2Fe-2S] center J. Bacteriol. 177 1995 2576 2582
78. T. Iwasaki, and T. Oshima Role of cytochrome b562 in the archaeal aerobic respiratory chain of Sulfolobus sp. strain 7 FEMS Microbiol. Lett. 144 1996 259 266
79. T. Iwasaki, K. Matsuura, and T. Oshima Resolution of the aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7: I. The archaeal terminal oxidase supercomplex is a functional fusion of respiratory complexes III and I V with no c-type cytochromes J. Biol. Chem. 270 1995 30881 30892
80. F. Baymann, E. Lebrun, M. Brugna, B. Schoepp-Cothenet, M.T. Giudici-Orticoni, and W. Nitschke The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes Philos. Trans. R. Soc. Lond., B Biol. Sci. 358 2003 267 274
81. J. Thompson, T. Gibson, F. Plewniak, F. Jeanmougin, and D. Higgins The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res. 25 1997 4876 4882