Abstract
A transcription unit petCB from Chlorobium limicola is described. The leading gene petC codes for a Rieske FeS-protein of 19.04 kDa with 181 amino acid residues. The following gene petB codes for a cytochrome b of 47.48 kDa with 428 amino acid residues. The transcription unit lacks a third gene pet-A for cytochrome c 1 or-f, which is found in the fbc-operons of gram-negative bacteria. In the derived amino acid sequence for the Rieske FeS-protein the four cysteines and the 2 histidines are conserved in the peptides binding the 2Fe2S-cluster, although the redox potential of the cluster is about 150 mV more negative in Chlorobium. The gene for cytochrome b includes the coding region for an N-terminal, positively charged extension which is typical for Chlorobium. The gene is not split into two parts for cytochrome b 6 and subunit IV. However, a fourteenth amino acid between the two histidines in the fourth, putative transmembrane helix, and the lack of an eighth transmembrane helix at the C-terminus, among other features, clearly resemble the cytochrome b 6 f-complexes. Therefore, the separation into b 6 f- and bc 1-type complexes during evolution must have occurred before the split of the gene.
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Beckmann, JD, Ljungdahl, PO, Lopez, JL and Trumpower, BL (1987) Isolation and characterization of the nuclear gene encoding the Rieske FeS-protein (RIP1) from Saccharomyces cerevisiae. J Biol Chem 262: 8901–8909
Blankenship, RE (1985) Electron transport in green photosynthetic bacteria. Photosynth Res 6: 317–333
Botstein D and Davis RW (1982) Principles and practice of recombinant DNA research with yeast. In: Strathern JN, Jones EW and Broach JR (eds) Molecular Biology of the Yeast Saccharomyces, pp 607–636. Cold Spring Harbor, New York
Büschlen, S, Choquet, Y, Kuras, R and Wollmann, F-A (1991) Nucleotide sequences of the continuous and separated petA, petB and petD chloroplast genes in Chlamydomonas reinhardii. FEBS Lett 284: 257–262
Büttner, M, Xie, D-L, Nelson, H, Pinther, W, Hauska, G and Nelson, N (1992) Photosythetic reaction center genes in green sulfur bacteria and in Photosystem 1 are related. Proc Natl Acad Sci USA 89: 8135–8139
Cabral, F and Schatz, G (1979) High resolution one- and two-dimensional electrophoretic analysis of mitochondrial membrane polypeptides. Methods Enzymol 56: 602–613
Cramer, WA, Black, MT, Widger, WR and Girvin, ME (1987) Stucture and functions of cytochrome bc 1 and b 6 f-complexes. In: Barber, J (ed) The Light Reactions, pp 447–493. Elsevier Science Publishers, Amsterdam
Crofts, AR, Hacker, B, Barquera, B, Yun, C-H and Gennis, R (1992) Stucture and function of the bc-complex of Rhodobacter sphaeroides. Biochim Biophys Acta 1101: 162–165
Dalbey, RE (1990) Positively charged residues are important determinants of membrane protein topology. Trends Biochem Sci 15: 253–257
Davidson, E and Daldal, F (1987) Primary structure of the cytochrome bc 1 complex of Rodopseudomonas capsulata. Nucleotide sequence of the pet operon encoding the Rieske, cytochrome b and cytochrome c 1 apoproteins. J Mol Biol 195: 13–24
Degli Esposti, M, De Vries, S, Crimi, M, Gelli, A, Patarnello, T and Meyer, A (1993) Mitochondrial cytochrome b: Evolution and stucture of the protein. Biochim Biophys Acta 1143: 243–271
Di Rago, J-P and Colson, A-M (1988) Molecular basis for resistance to antimycin A 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
Di Rago, J-P, Coppée, J-Y and Colson, A-M (1988) Molecular basis for resistance to myxothiazol, muicidin (strobilurin A) and stigmatellin, cytochrome b inhibitors acting at the center o of the Saccharomyces cerevisiae. J Biol Chem 264: 14543–14548
Gabellini, N and Sebald, W (1986) Nucleotide sequence and transcription of the fbc operon from Rhodopseudomonas sphaeroides. Eur J Biochem 154: 569–579
Hallick, RB (1989) Proposals for the naming of chloroplast genes. Plant Mol Biol Rep 7: 266–275
Hauska, G, Hurt, E, Gabellini, N and Lockau, W (1983) Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim Biophys Acta 726: 97–133
Hauska, G, Nitschke, W and Herrmann, RG (1988) Amino acid identitles in the three redox center-carrying polypeptides of cytochrome bc 1/b 6 f complexes. J Bioenerg Biomembr 20: 211–228
Heinemeyer, W, Alt, J and Herrmann, RG (1984) Nucleotide sequence of the clustered genes for apocytochrome b 6 and subunit 4 of the cytochrome bf complex in the spinach plastid chromosome. Curr Genet 8: 543–549
Henikoff, S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351–359
Howell, N and Gilbert, K (1988) Mutational analysis of the mouse mitochondrial cytochrome b gene. J Mol Biol 203: 607–618
Hurt, EC and Hauska, G (1984) Purification of membrane-bound cytochromes and a photoactive P840 protein complex of the green sulfur bacterium Chlorobium limicola f. thiosulfatophllum. FEBS Lett 168: 149–154
Ikeuchi, M, Hirano, A, Hlyama, T and Inoue, Y (1990) Polypeptide composition of higher plant Photosystem I complex. FEBS Lett 263: 274–278
Kallas, T, Spiller, S and Malkin, R (1988a) Primary stucture of cotranscriped genes encoding the Rieske FeS and Cytochrome f proteins of the cyanobacterium Nostoc PCC 7906. Proc Natl Acad Sci USA 85: 5794–5798
Kallas, T, Spiller, S and Malkin, R (1988b) Characterization of two operons encoding the cytochrome b 6 f-complex of the cyanobacterium Nostoc PCC 7906. J Biol Chem 263: 14334–14342
Knaff, DB and Buchanan, BB (1975) Cytochrome b and photosynthetic sulfur bacteria. Biochim Biophys Acta 376: 549–560
Knaff, DB and Malkin, R (1976) Iron-sulfur proteins of the green photosynthetic bacterium Chlorobium. Biochim Biophys Acta 430: 244–252
Koike, K, Kobayashi, M, Yaginuma, K, Taira, M, Yoshida, E and Imai, M (1982) Nucleotide sequence and evolution of the rat mitochondrial cytochrome b gene containing the ochre termination codon. Gene 20: 177–185
Kurowski, B and Ludwig, B (1987) The genes of the Paracoccus denitrificans bc 1 complex. J Biol Chem 262: 13805–13811
Kutoh, E and Sone, N (1988) Quinol-cytochrome e oxido-reductase from the thermophilic bacterium PS3. Purification and properties of a cytochrome bc 1(b 6 f) complex. J Biol Chem 263: 9020–9026
Laemmli, UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685
Majewski, C and Trebst, A (1990) The pet genes of Rhodospirillm rubrum: Cloning and sequencing of the genes for the cytochrome bc 1-complex. Mol Gen Genet 224: 373–382
Matsudaira, P (1987) Sequence from picomole quantities of proteins eletroblotted onto polyvinylidene difluoride membranes. J Biol Chem 262: 10035–10038
Mayes and Barber (1991) Primary structure of the psbN-psbH-petC-petA gene cluster of the cyanobacterium Synechocystis PCC 6803. Plant Mol Biol 17: 289–293
Mitchell, P (1976) Possible mechanism of the protonmotive function of cytochrome systems. J Theor Biol 62: 327–367
Nishikimi et al. (1989) Cloning and sequence analysis of cDNA encoding the Rieske iron-sulfur protein of rat mitochondrial cytochrome bc 1 complex. Biochem Biophys Res Comm 159: 19–25
Nobrega, FG and Tzagoloff, A (1980) Assembly of the mitochondrial membrane system. DNA sequence and organization of the cytochrome b gene in Saccharomyces cerevisiae. J Biol Chem 255: 9828–9837
Oettmeier, W, Godde, D, Kunze, B and Höfle, G (1985) Stigmatellin, a dual type inhibitor of photosynthetic electron transport. Biochim Biophys Acta 807: 216–219
Ohyama, K, Fukuzawa, H, Kohchi, T, Shirai, H, Sano, T, Sano, S, Umesono, K, Shiki, Y, Takeuchi, M, Chang, Z, Aota, S, Inokuchi, H and Ozeki, H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–575
Okkels, JS, Kjaer, B, Hansson, Ö, Svendsen, I, Lindberg-Möller, B and Scheller, HV (1992) A membrane-bound monoheme cytochrome c-551 of a novel type is the immediate electron donor to P840 of the Chlorobium vibrioforme photosynthetic reaction center. J Biol Chem 267: 21139–21145
Robertson, DE, Daldal, F and Dutton, PL (1990) Mutants of ubiquinol-cytochrome c2 oxidoreductase resistant to Qo site inhibitors: Consequenees for ubiquinone and ubiquinol affinity and catalysis. Biochemistry 29: 11249–11260
Salter, AH, Newman, BJ, Napier, JA and Gray, JC (1992) Characterisation of cDNA clones encoding the precursor of the Rieske iron-sulfur protein of pea chloroplasts. Plant Mol Biol 20: 569–574
Sambrook, J, Fritsch, EF and Maniatis, T (1989) Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Publ, New York
Steppuhn, J, Hermans, J, Jansen, T, Salnikow, J, Hauska, G and Herrmann, RG (1987) The complete amino acid sequence of the Rieske FeS-precursor protein from spinach chloroplasts deduced from cDNA analysis. Mol Gen Genet 210: 171–177
Thomas, PE, Ryan, C and Levin, W (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75: 168–176
Von Jagow, G and Link, TA (1986) Use of specific inhibitors on the mitochondrial bc 1-complex. Methods Enzymol 126: 253–271
Wachleitner, JA and Wolstenholme, DR (1988) Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucleic Acids Res 16: 6897–6913
Woese, CR (1987) Bacterial evolution. Microbiol Rev 51: 221–271
Xie, D-L, Lill, H, Hauska, G, Maeda, M, Futai, M and Nelson, N (1993) The apt2 operon of the green bacterium Chlorobium limicola. Biochim Biophys Acta 1172: 267–273
Yun, C-H, Beci, R, Crofts, AR, Kaplan, S and Gennis, RB (1990) Cloning and DNA sequencing of the fbc operon encoding the cytochrome bc 1 complex from Rhodobacter sphaeroides. Characterization of fbc deletion mutants and complementation by a site-specific mutational varian. Eur J Biochem 194: 399–411
Zirngibl, S, Xie, D-L, Riedel, A, Nitschke, W, Nelson, H, Nelson, N, Liebl, U, le Coutre, J, Hauska, G, Kellner, E, Grodzitzki, D and Büttner, M (1992) Low potential Rieske FeS-centers of menaquinol oxidizing cytochrome bc-complexes. In: Murata, N (ed) Research in Photosynthesis, Vol II, pp 471–478. Kluwer Academic Publishers, Dordrecht, The Netherlands
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Dedicated to Achim Trebst on the occasion of his 65th birthday.
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Schütz, M., Zirngibl, S., le Coutre, J. et al. A transcription unit for the Rieske FeS-protein and cytochrome b in Chlorobium limicola . Photosynth Res 39, 163–174 (1994). https://doi.org/10.1007/BF00029383
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DOI: https://doi.org/10.1007/BF00029383