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The pet operon, encoding the prosthetic group-containing subunits of the cytochrome bc1 complex, of the purple sulfur bacterium Chromatium vinosum

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Abstract

The pet operon, encoding the prosthetic group-containing subunits of the cytochrome bc 1 complex of the purple sulfur bacterium Chromatium vinosum, has been cloned and sequenced. The 5′ to 3′ order of the C. vinosum genes is: petA, encoding the Rieske iron-sulfur protein; petB, encoding cytochrome b; and petC, encoding cytochrome c1. Cytochrome b is the best conserved subunit of the C. vinosum complex, when compared to the corresponding proteins from four photosynthetic purple non-sulfur bacteria (70 to 74% identity). Identities for the C. vinosum Rieske protein and those from purple non-sulfur bacteria range from 60 to 64%. The C-terminal region of the C. vinosum Rieske protein is quite similar to those of purple non-sulfur bacteria, while the N-terminal region is more closely related to mitochondrial Rieske proteins of organisms such as Neurospora crassa. Cytochrome c1 is the least well-conserved protein of the C. vinosum cytochrome bc1 complex, with identities ranging from 49 to 51% when compared to the corresponding proteins from purple non-sulfur bacteria. A well-conserved negatively-charged region of the cytochromes c1 of the purple non-sulfur bacteria, thought to be involved in binding the electron acceptor for the complex, cytochrome c2, is absent in C. vinosum cytochrome c1. A positive Southern hybridization using a probe constructed from the Rhodobacter sphaeroides fbcQ gene, which codes for a fourth subunit of the cytochrome bc1 complex in that bacterium, suggests the presence of a homologous gene in C. vinosum.

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References

  • Andrews KM, Crofts AR and Gennis RB (1990) Large-scale purification and characterization of a highly active four-subunit cytochrome bc 1 complex from Rhodobacter sphaeroides. Biochemistry 29: 2645–2651

    Google Scholar 

  • Atteia A and Franzen LG (1996) Identification, cDNA sequence and deduced amino acid sequence of the mitochondrial Rieske iron–sulfur protein from the green alga Chlamydomonas reinhardtii. Implications for protein targeting and subunit interaction. Eur J Biochem 237: 792–799

    Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Steidman JG, Smith JA and Strihl K (1987) Current Protocols in Molecular Biology. John Wiley & Sons, New York

    Google Scholar 

  • Axelrod HL, Feher G, Allen JP, Chirino AJ, Day MW, Hsu BT and Rees DR (1994) Crystallization and x-ray structure determination of cytochrome c 2 from Rhodobacter sphaeroides in three crystal forms. Acta Cryst D50: 596–602

    Google Scholar 

  • Benning MM, Wesenberg G, Caffrey MS, Bartsch RG, Meyer TE, Cusanovich MA, Rayment I and Holden HM (1991) Molecular structure of cytochrome c 2 isolated from Rhodobacter capsulatus determined at 2.5 Å resolution. J Mol Biol 220: 673–685

    Google Scholar 

  • Benning MM, Meyer TE and Holden HM (1996) Molecular structure of a high potential cytochrome c 2 isolated from Rhodophila globiformis. Arch Biochem Biophys 333: 338–348

    Google Scholar 

  • Bowyer JR and Crofts AR (1980) The photosynthetic electron transfer chain of Chromatium vinosum chromatophores. Flashinduced cytochrome b reduction. Biochim Biophys Acta 591: 298–311

    Google Scholar 

  • Brandt U and Trumpower BL (1994) The protonmotive Q cycle in mitochondria and bacteria. Crit Rev Biochem Molec Biol 29: 165–197

    Google Scholar 

  • Brasseur R (1988) Calculation of the three-dimensional structure of Saccharomyces cerevisiae cytochrome b inserted in a lipid matrix. J Biol Chem 263: 12571–12575

    Google Scholar 

  • Brasseur G, Sled V, Liebl U, Ohnishi T and Daldal F (1997) The amino terminal portion of the Rieske iron–sulfur protein contributes to the ubihydroquinone oxidation site catalysis of the Rhodobacter capsulatus bc 1 complex. Bicohemistry 36: 11685–11696

    Google Scholar 

  • Britt RD, Sauer K, Klein MP, Knaff DB, Kriauciunas A, Yu C-A, Yu L and Malkin R (1991) Electron spin echo envelope modulation spectroscopy supports the suggested coordination of two histidine ligands to the Rieske Fe–S centers of the cytochrome b 6 f complex of spinach and the cytochrome bc 1 complexes of Rhodospirillum rubrum, Rhodobacter sphaeroides R-26, and bovine heart mitochondria. Biochemistry: 30: 1892–1901

    Google Scholar 

  • Broger C, Salardi S and Azzi A (1983) Interaction between isolated cytochrome c 1 and cytochrome c. Eur J Biochem 131: 349–352

    Google Scholar 

  • Chen YL (1996) Characterization of the cytochrome bc 1 complex pet genes from Chromatium vinosum. PhD Dissertation, Texas Tech University

  • Chen Y-R, Shenoy SK, Yu C-A and Yu L (1995) Identification of amino acid residues involved in structural and ubiquinone binding functions of Subunit IV of the cytochrome bc 1 complex from Rhodobacter sphaeroides. J Biol Chem 270: 11496–11501

    Google Scholar 

  • Coremans JMCC, Van der Wal HN, Van Grondelle R, Amesz J and Knaff DB (1985) The pathway of cyclic electron transport in chromatophores of Chromatium vinosum. Evidence for a Q-Cycle mechanism. Biochim Biophys Acta 807: 134–142

    Google Scholar 

  • Crofts A, Robinson H, Andrews K, Van Doren S and Berry E (1987) Catalytic sites for reduction and oxidation of quinones. In: Papa S, Chance B and Ernster L (eds) Cytochrome Systems, pp 617–624. Plenum Press, New York

    Google Scholar 

  • Cully M, Jay FA, Gabellini N and Oesterhelt D (1989) Characterization of the bc 1 complex in Rhodopseudomonas viridis. In: Barber J and Malkin R (eds) Techniques and New Developments in Photosynthesis Research, pp 287–289. Plenum Press, New York

    Google Scholar 

  • Daldal F, Tokito MK, Davidson E and Faham M (1989) Mutations conferring resistance to quinol oxidation (Qz)-inhibitors of the cytochrome bc 1 complex of Rhodobacter capsulatus. EMBO J 8: 3951–3961

    Google Scholar 

  • Davidson E and Daldal F (1987a) Primary structure of the bc 1 complex of Rhodopseudomonas capsulata. J Mol Biol 195: 13–24

    Google Scholar 

  • Davidson E and Daldal F (1987b) fbc operon, encoding the Rieske Fe–S protein, cytochrome b and cytochrome c 1 apoproteins previously described from Rhodopseudomonas sphaeroides, is from Rhodopseudomonas capsulata. J Mol Biol 195: 25–29

    Google Scholar 

  • Davidson E, Ohnishi T, Atta-Asafo-Adjei E and Daldal F (1992) Potential ligands to the [2Fe–2S] Rieske cluster of the cytochrome bc 1 complex of Rhodobacter capsulatus probed by site-directed mutagenesis. Biochemistry 31: 3342–3351

    Google Scholar 

  • Di Rago JP and Colson AM (1988) Molecular basis for resistance to antimycin and diuron, Q-cycle inhibitors acting at the Qi site in the mitochondrial ubiquinol-cytochrome c reductase in Saccharomyces cerevisiae. J Biol Chem 263: 12564–12570

    Google Scholar 

  • Di Rago JP, Coppee JY and Colson AM (1989) Molecular basis for resistance to myxothiazol, mucidin (strobilurin a) and stigmatellin. J Biol Chem 264: 14543–14548

    Google Scholar 

  • Dutton PL and Leigh JS (1973) Electron spin resonance characterization of Chromatium D hemes, non-heme irons and the components involved in primary photochemistry. Biochim Biophys Acta 314: 178–190

    Google Scholar 

  • Evans MCW, Lord AV and Reeves SG (1974) The detection and characterization by electron-paramagnetic-resonance spectroscopy of iron–sulfur proteins and other electron-transport components in chromatophores from the purple bacterium Chromatium. Biochem J 138: 177–183

    Google Scholar 

  • Finnegan MG, Knaff DB, Qin H, Gray KA, Daldal F, Yu L, Yu CA, Kleis-SanFrancisco S and Johnson MK (1996) Axial heme ligation in the cytochrome bc 1 complexes of mitochondrial and photosynthetic membranes. A near-infrared magnetic circular dichroism and electron paramagnetic resonance study. Biochim Biophys Acta 1274: 9–20

    Google Scholar 

  • Gabellini N and Sebald W (1986) Nucleotide sequence and transcription of the fbc operon from Rhodopseudomonas sphaeroides. Eur J Biochem 154: 569–579

    Google Scholar 

  • Gaul DF and Knaff DB (1983) The presence of cytochrome c 1 in the purple sulfur bacterium Chromatium vinosum. FEBS Lett 162: 69–74

    Google Scholar 

  • Gray KA and Daldal F (1995) Mutational studies of the cytochrome bc 1 complexes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 747–774. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Gray KA, Davidson E and Daldal F (1992) Mutagenesis of methionine-183 drastically affects the physicochemical properties of cytochrome c 1 of the bc 1 complex of Rhodobacter capsulatus. Biochemistry 31: 11864–11873

    Google Scholar 

  • Groisman EA, Saier, Jr. MH and Ochman H (1992) Horizontal transfer of a phosphatase gene as evidence for mosaic structure of the Salmonella genome. EMBO J 11: 1309–1316

    Google Scholar 

  • Güner S, Willie A, Millett F, Caffrey MS, Cusanovich MA, Robertson DE and Knaff DB (1993) The interaction between cytochrome c 2 and the cytochrome bc 1 complex in the photosynthetic purple bacteria Rhodobacter capsulatus and Rhodopseudomonas viridis. Biochemistry 32: 4793–4800

    Google Scholar 

  • Gurbiel RJ, Ohnishi T, Robertson DE, Daldal F and Hoffman BM (1991) Q-band ENDOR spectra of the Rieske protein from Rhodobacter capsulatus ubiquinol-cytochrome c oxidoreductase show two histidines coordinated to the [2Fe–2S] cluster. Biochemistry 30: 11579–11584

    Google Scholar 

  • Guiseppi A, Aymeric JL, Cami B, Barras F and Creuzet N (1991) Sequence analysis of the cellulase-encoding celY gene of Erwinia chrysantemi: A possible case of interspecies gene transfer. Gene 106: 109–114

    Google Scholar 

  • Howell N and Gilbert K (1988) Mutational analysis of the mouse mitochondrial cytochrome b gene. J Mol Biol 203: 607–618

    Google Scholar 

  • Iwata S, Saynovits M, Links TA and Michel H (1996) Structure of the water soluble fragment of the 'Rieske' iron–sulfur protein of the bovine heart mitochondrial cytochrome bc 1 complex determined by MAD phasing at 1.5 Å resolution. Structure 4: 567–579

    Google Scholar 

  • Kerfeld CA, Chan C, Hirasawa M, Kleis-SanFrancisco S, Yeates TO and Knaff DB (1996) Isolation and characterization of soluble electron transfer proteins from Chromatium purpuratum. Biochemistry 35: 7812–7818

    Google Scholar 

  • Knaff DB and Buchanan BB (1975) Cytochrome b and photosynthetic sulfur bacteria. Biochim Biophys Acta 376: 549–560

    Google Scholar 

  • Konishi K, Van Doren SR, Kramer DM, Crofts AR and Gennis RB (1991) Preparation and characterization of the water-soluble heme-binding domain of cytochrome c 1 from the Rhodobacter sphaeroides bc 1 complex. J Biol Chem 266: 14270–14276

    Google Scholar 

  • Kriauciunas A, Yu L, Yu C-A, Wynn RM and Knaff DB (1989) The Rhodospirillum rubrum cytochrome bc 1 complex: Peptide composition, prosthetic group content and quinone binding. Biochim Biophys Acta 976: 70–76

    Google Scholar 

  • Kyte J and Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132

    Google Scholar 

  • Liebl U, Sled V, Brasseur G, Ohnishi T and Daldal F (1997) Conserved non-liganding residues of the Rhodobacter capsulatus Rieske iron–sulfur protein of the bc 1 complex are essential for protein structure, properties of the [2Fe–2S] cluster, and communication with the quinone pool. Biochemistry 36: 11675–11684

    Google Scholar 

  • Link TA, Saynovits M, Assmann C, Iwata S, Ohnishi T and Von Jagow G (1996) Isolation, characterization and crystallization of a water-soluble fragment of the Rieske iron–sulfur protein of bovine heart mitochondrial bc 1 complex. Eur J Biochem 237: 71–75

    Google Scholar 

  • Majewski C and Trebst A (1990) The pet genes of Rhodospirillum rubrum: Cloning and sequencing of the genes for the cytochrome bc 1 complex. Mol Gen Genet 224: 373–382

    Google Scholar 

  • Malkin, R (1992) Cytochrome bc 1 and b 6 f complexes of photosynthetic membranes. Photosynth Res 33: 121–136

    Google Scholar 

  • Meinhardt SW and Crofts AR (1982) Kinetic and thermodynamic resolution of cytochrome c 1 and cytochrome c 2 from Rhodopseudomonas sphaeroides. FEBS Lett 149: 223–227

    Google Scholar 

  • Menin L, Gaillard J, Parot P, Schoepp B, Nitschke W and Verméglio A (1998) Role of HiPIP as electron donor to the RC-bound cytochrome in photosynthetic purple bacteria. Photosynth Res 55(2-3): 343–348

    Google Scholar 

  • Meyer TE and Donohue TJ (1995) Cytochromes, iron–sulfur, and copper proteins mediating electron transfer from the cyt bc 1 complex to photosynthetic reaction center complexes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 725–745. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Platt T and Bear DG (1983) Role of RNA polymerase, factors and ribosomes in transcription termination. In: Beckwith J, Davies J and Gallant JA (eds) Gene function in prokaryotes pp 123–161. Cold Spring Harbour Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Purvis DJ, Theiler R and Neiderman RA (1990) Chromatographic and protein chemical analysis of the ubiquinol-cytochrome c 2 oxidoreductase isolated from Rhodobacter sphaeroides. J Biol Chem 265: 1208–1215

    Google Scholar 

  • Robertson DE, Ding H, Chelminski PR, Slaughter C, Hsu J, Moomaw C, Tokito M, Daldal F and Dutton PL (1993) Hydroubiquinone-cytochrome c 2 oxidoreductase from Rhodobacter capsulatus: Definition of a minimal, functional isolated preparation. Biochemistry 32: 1310–1317

    Google Scholar 

  • Salemme FR, Freer ST, Xuong NH, Alden RA and Kraut J (1973) The structure of oxidized cytocrome c 2 of Rhodospirillum rubrum. J Biol Chem 248: 3910–3921

    Google Scholar 

  • Sambrook J, Fritsch E and Maniatis T (1989) Molecular Cloning – A Laboratory Manual. Cold Spring Harbor Press, New York

    Google Scholar 

  • Samyn B, De Smet L, Van Driessche G, Meyer TE, Bartsch RG, Cusanovich MA and Van Beeumen JJ (1996) A high-potential soluble cytochrome c-551 from the purple phototrophic bacterium Chromatium vinosum is homologous to cytochrome c 8 from denitrifying pseudomonads. Eur J Biochem 236: 689–696

    Google Scholar 

  • Sanger F, Nicklen S and Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    Google Scholar 

  • Shanker S, Moomaw C, Güner S, Hsu J, Tokito MK, Daldal F, Knaff D B and Harman JG (1992) Characterization of the pet operon of Rhodospirillum rubrum. Photosynth Res 32: 79–94

    Google Scholar 

  • Sogabe S and Miki K (1995) Refined crystal structure of ferrocytochrome c 2 from Rhodopseudomonas viridis at 1.6 Å resolution. J Mol Biol 252: 235–247

    Google Scholar 

  • Sone N, Tsuchiya N, Inoue M and Noguchi S (1996) Bacillus stearothermophilus qcr operon encoding Rieske FeS protein, cytochrome b 6, and a novel-type cytochrome c 1 of quinolcytochrome c reductase. J Biol Chem 271: 12457–12462

    Google Scholar 

  • Stonehuerner J, O'Brien P, Geren L, Millett F, Steidl J, Yu L and Yu C-A (1985) Identification of the binding site on cytochrome c 1 for cytochrome c. J Biol Chem 260: 5392–5398

    Google Scholar 

  • Swofford DL (1990) PAUP: Phylogenetic analysis using parsimony, Version 3.0. Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  • Takamiya K (1980) Interaction between antimycin and cytochrome b 560 in Chromatium chromatophores – the red shift of the absorption spectrum and photoreduction of cytochrome b 560 in the presence of antimycin. Plant Cell Physiol 21: 1551–1557

    Google Scholar 

  • Takamiya K and Hanada (1980) Cytochrome b 560 in chromatophores from Chromatium vinosum. Plant Cell Physiol 21: 979–988

    Google Scholar 

  • Tan J, Corson GE, Chen YL, Garcia MC, Güner S and Knaff DB (1993) The ubiquinol: cytochrome c 2/c oxidoreductase of Chromatium vinosum. Biochim Biophys Acta 1144: 69–76

    Google Scholar 

  • Tian H, Yu L, Mather MW and Yu C-A (1997) The involvement of serine 175 and alanine 185 of cytochrome b of Rhodobacter sphaeroides cytochrome bc 1 in interaction with iron–sulfur protein. J Biol Chem 272: 23722–23728

    Google Scholar 

  • Usui S and Yu L (1991) Subunit IV (Mr = 14,384) of the cytochrome b-c 1 complex from Rhodobacter sphaeroides. J Biol Chem 266: 15644–15649

    Google Scholar 

  • Van Doren SR, Gennis RB, Barquera B and Crofts AR (1993a) Site-directed mutations of conserved residues of the Rieske iron–sulfur subunit of the cytochrome bc 1 complex of Rhodobacter sphaeroides blocking or impairing quinol oxidation. Biochemistry 32: 8083–8091

    Google Scholar 

  • Van Doren SR, Yun C-H, Crofts AR and Gennis RB (1993b) Assembly of the Rieske iron–sulfur subunit of the cytochrome bc 1 complex in the Escherichia coli and Rhodobacter sphaeroides membranes independent of the cytochrome b and c 1 subunits. Biochemistry 32: 628–636

    Google Scholar 

  • Van Heijne G (1988) Transcending the inpenetrable: How proteins come to terms with membranes. Biochim Biophys Acta 947: 307–333

    Google Scholar 

  • Verbist J, Lang F, Gabellini N and Oesterhelt D (1989) Cloning and sequencing of the fbcF, B and C genes encoding the cytochrome b/c 1 complex from Rhodopseudomonas viridis. Mol Gen Genet 219: 445–452

    Google Scholar 

  • Xia D, Yu C-A, Kim H, Xia J-Z, Kachurin AM, Zhang L, Yu L and Deisenhofer J (1997) Crystal structure of the cytochrome bc 1 complex from bovine heart mitochondria. Science 277: 60–66

    Google Scholar 

  • Yu L and Yu C-A (1991) Essentiality of the molecular weight 15 000 protein (Subunit IV) in the cytochrome b-c 1 complex of Rhodobacter sphaeroides. Biochemistry 30: 4934–4939

    Google Scholar 

  • Yu L, Mei Q-C and Yu C-A (1984) Characterization of purified cytochrome b-c 1 complex from Rhodopseudomonas sphaeroides R-26. J Biol Chem 259: 5752–5760

    Google Scholar 

  • Yu C-A, Xia J-Z, Kachurin AM, Yu L, Xia D, Kim H and Deisenhofer J (1996) Crystallization and preliminary structure of beef heart mitochondrial cytochrome-bc 1 complex. Biochim Biophys Acta 1275: 47–53

    Google Scholar 

  • Yun C-H, Beci R, Crofts AR, Kaplan S and Gennis RB (1990) Cloning and sequencing of the fbc operon encoding the cytochrome bc 1 complex from Rhodobacter sphaeroides. Eur J Biochem 194: 399–411

    Google Scholar 

  • Yun C-H, Van Dorn, SR, Crofts AR and Gennis RB (1991a) The use of gene fusions to examine membrane topology of the L-subunit of the photosynthetic reaction center and of the cytochrome b subunit of the bc 1 complex from Rhodobacter sphaeroides. J Biol Chem 266: 10967–10973

    Google Scholar 

  • Yun C-H, Crofts AR and Gennis RB (1991b) Assignment of the histidine axial ligands to the cytochrome b H and cytochrome b L components of the cytochrome bc 1 complex from Rhodobacter sphaeroides by site-directed mutagenesis. Biochemistry 30: 6747–6754

    Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi Y, Kim KK, Hung L-W, Crofts AR, Berry EA and Kim S-H (1998) Electron transfer by domain movement in cytochrome bc 1. Nature 392: 677–684.

    Google Scholar 

  • Zuker M (1989) On finding all suboptimal folding of an RNA molecule. Science 244: 48–52

    Google Scholar 

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Chen, Y.L., Benan Dincturk, H., Qin, H. et al. The pet operon, encoding the prosthetic group-containing subunits of the cytochrome bc1 complex, of the purple sulfur bacterium Chromatium vinosum. Photosynthesis Research 57, 139–158 (1998). https://doi.org/10.1023/A:1006052408216

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