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Cytochrome bc 1 and b 6 f complexes of photosynthetic membranes

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Abstract

All photosynthetic membranes contain a cytochrome bc 1 or b 6 f complex that catalyzes the oxidation of quinols and the reduction of a high-potential electron carrier, such as cytochrome c 2 or plastocyanin. The cytochrome complex also functions in the translocation of protons across the membrane and as a consequence, establishes the proton motive force that is used for the synthesis of ATP. The structure and function of the cytochrome complexes are first reviewed in this chapter. Amino acid sequence information for almost all of the protein subunits of these complexes is now available, and these allow for a detailed consideration of functional domains in the protein subunits and for a further discussion of the evolution of the cytochrome complex in photosynthetic organisms.

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References

  • Adam Z and Malkin R (1987) Reconstitution of isolated Rieske Fe-S protein into a Rieske-depleted cytochrome b 6 f complex. FEBS Lett 225: 67–71

    Article  PubMed  Google Scholar 

  • Baroli I, Fernandez-Velasco J and Crofts AR (1991) Spectral and thermodynamic characterization of cytochrome b in stroma vesicles from spinach chloroplasts. Biophys J 59: 145a

  • 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 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

    PubMed  Google Scholar 

  • Carter KR, T'sai A-L and Palmer G (1981) The coordination environment of mitochondrial cytochrome b. FEBS Lett 132: 243–246

    Article  PubMed  Google Scholar 

  • Cline JF, Hoffmann BM, Mims WB, LaHaie E, Ballou DP and Fee JA (1985) Evidence for N coordination to Fe in the [2Fe-2S] clusters of Thermus Rieske protein and phthalate dioxygenase from Pseudomonas. J Biol Chem 260: 3251–3254

    PubMed  Google Scholar 

  • Cramer WA, Black MT, Widger WR and Girvin ME (1987) Structure and function of the photosynthetic cytochrome bc 1 and b 6 f complexes. In: Barber J (ed) The Light Reactions, pp 447–493. Elsevier Science Publishing, Inc., New York

    Google Scholar 

  • Daldal F, Davidson E and Cheng S (1987) Isolation of the structural genes for the Rieske Fe-S protein, cytochrome b and cytochrome c 1 — all components of the ubiquinol-cytochrome c 2 oxidoreductase complex of Rhodopseudomonas capsulata. J Mol Biol 195: 1–12

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • deVries S and Marres CAM (1987) The mitochondrial respiratory chain of yeast. Structure and biosynthesis and the role in cellular metabolism. Biochim Biophys Acta 895: 205–239

    PubMed  Google Scholar 

  • DiRago 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

    PubMed  Google Scholar 

  • DiRago JP, Coppee JY and Colson AM (1989) Molecular basis for resistance to myxothiazole, mucidin (strobilurin A), and stigmatellin. Cytochrome b inhibitors acting as the center o of the mitochondrial ubiquinol-cytochrome c reductase in Saccharomyces cerevisiae. J Biol Chem 264: 14543–14548

    PubMed  Google Scholar 

  • Doyle M, Li L-B, Yu C-A (1989) Identification of a Mr=17000 protein as the plastoquinone-binding protein in the cytochrome b 6 f complex from spinach chloroplasts. J Biol Chem 264: 1387–1392

    PubMed  Google Scholar 

  • Erecinska M, Chance B, Wilson DF and Dutton PL (1972) Aerobic reduction of cytochrome b 566 in pigeon-heart mitochondria. Proc Natl Acad Sci USA 69: 50–54

    PubMed  Google Scholar 

  • Gabellini N (1988) Organization and structure of the genes for the cytochrome bc 1 complex in purple photosynthetic bacteria. A phylogenetic study describing the homology of the bc 1 subunits between prokaryotes, mitochondria and chloroplasts. J Bioenerg Biomembr 20: 59–83

    PubMed  Google Scholar 

  • Gabellini N, Bowyer JR, Hurt E, Melandri BA and Hauska G (1982) A cytochrome bc 1 complex with ubiquinol-cytochrome c 2; oxidoreductase activity from Rhodopseudomonas sphaeroides GA. Eur J Biochem 126: 105–111

    PubMed  Google Scholar 

  • Gonzalez-Halphen D, Vazquez-Acevedo M and Garcia-Ponce B (1991) On the interaction of mitochondrial complex III with the Rieske iron-sulfur protein (subunit V). J Biol Chem 266: 3870–3876

    PubMed  Google Scholar 

  • Haley J and Bogorad L (1989) A 4-kDa maize chloroplast polypeptide associated with the cytochrome b 6 f complex: subunit 5, encoded by the chloroplast petE gene. Proc Natl Acad Sci USA 86: 1534–1538

    PubMed  Google Scholar 

  • Hartl F, Schmidt B, Wachter E, Weiss H and Neupert W (1986) Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell 47: 939–951

    Article  PubMed  Google Scholar 

  • Hauska G (1986) Composition and structure of cytochrome bc and b 6 f complexes. In: Staehelin LA and Arntzen CJ (eds) Photosynthesis III. Photosynthetic Membranes and Light Harvesting Systems, pp 496–507. Springer-Verlag, Berlin

    Google Scholar 

  • Hauska G, Hurt E, Gabellini N and Lockau W (1983) Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim. Biophys Acta 726: 97–133

    PubMed  Google Scholar 

  • Hauska G, Nitschke W and Herrmann RG (1988) Amino acid identities in the three redox center-carrying polypeptides of the cytochrome bc 1/b 6 f complexes. J Bioenerg Biomembr 20: 211–228

    PubMed  Google Scholar 

  • Howell N (1989) Evolutionary conservation of protein regions in the protonmotive cytochrome b and their posible roles in redox catalysis. J Mol Evol 29: 157–169

    PubMed  Google Scholar 

  • Hurt E and Hauska G (1981) A cytochrome f/b 6 complex of five polypeptides with plastoquinol-plastocyanin-oxidoreductase activity from spinach chloroplasts. Eur J Biochem 117: 591–599

    PubMed  Google Scholar 

  • Hurt E and Hauska G (1982a) Identification of polypeptides in the cytochrome b 6 f complex from spinach chloroplasts with redox-center-carrying subunits. J Bioenerg Biomembr 14: 405–424

    PubMed  Google Scholar 

  • Hurt E and Hauska G (1982b) Oxidant-induced reduction of cytochrome b 6 in isolated cytochrome b 6 f complex from chloroplasts. Photobiochem Photobiophys 4: 9–15

    Google Scholar 

  • Hurt E and Hauska G (1983) Cytochrome b 6 from isolated cytochrome b 6 f complexes. Evidence for two spectral forms with different midpoint potentials. FEBS Lett 153: 413–419

    Article  Google Scholar 

  • Hurt EC, Gabellini N, Shahak Y, Lockau W and Hauska G (1983) Extra proton translocation and membrane potential generation-universal properties of cytochrome bc 1/b 6 f complexes reconstituted into liposomes. Arch Biochem Biophys 225: 879–885

    PubMed  Google Scholar 

  • Ingledew WJ, Reid GA, Poole RK, Blum H and Ohnishi T (1980) The iron-sulphur centres of aerobically-grown Escherichia coli K12. FEBS Lett 111: 223–227

    Article  PubMed  Google Scholar 

  • Kallas T, Spiller S and Malkin R (1988a) Characterization of two operons encoding the cytochrome b 6 f complex of the cyanobacterium Nostoc PCC 7906. Highly conserved sequences but different gene organization than in chloroplasts. J Biol Chem 263: 14334–14342

    PubMed  Google Scholar 

  • Kallas T, Spiller S and Malkin R (1988b) Primary structure of cotranscribed genes encoding the Rieske iron-sulfur protein and cytochrome f proteins of the cyanobacterium Nostoc PCC 7906. Proc Natl Acad Sci USA 85: 5794–5798

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Knaff DB and Malkin R (1976) Iron-sulfur proteins of the green photosynthetic bacterium, Chlorobium. Biochim Biophys Acta 430: 244–252

    PubMed  Google Scholar 

  • Krinner M, Hauska G, Hurt E and Lockau W (1982) A cytochrome f-b 6 complex with plastoquinol-cytochrome c oxidoreductase activity from Anabena variabilis. Biochim Biophys Acta 681: 110–117

    Google Scholar 

  • Kurowski B and Ludwig B (1987) The genes of the Paracoccus denitrificans bc 1 complex. Nucleotide sequence and homologies between bacterial and mitochondrial subunits. J Biol Chem 263: 13805–13811

    Google Scholar 

  • Kutoh E and Sone N (1988) Quinol-cytochrome c oxidoreductase from the thermophilic bacterium PS3. Purification and properties of a cytochrome bc 1 (b 6 f) complex. J Biol Chem 263: 9020–9026

    PubMed  Google Scholar 

  • Lewis RJ, Prince R, Dutton PL, Knaff DB and Krulwich TA (1981) The respiratory chain of Bacillus alcalophilus and its non-alkalophilic mutant derivative. J Biol Chem 256: 10543–10559

    PubMed  Google Scholar 

  • Ljungdahl PO, Pennoyer JD, Robertson DE and Trumpower BL (1987) Purification of highly active cytochrome bc 1 complexes from phylogenetically diverse species by a single chromatographic procedure. Biochim Biophys Acta 891: 227–241

    PubMed  Google Scholar 

  • Malkin R (1986) Interaction of stigmatellin and DNP-INT with the Rieske iron-sulfur center of the chloroplast cytochrome b 6 f complex. FEBS Lett 208: 317–320

    Article  PubMed  Google Scholar 

  • Malkin R (1988) Structure-function studies of photosynthetic cytochrome bc 1 and b 6 f complexes. ISI Atlas of Science-Biochemistry 1: 57–64

    Google Scholar 

  • Malkin R and Aparicio PJ (1975) Identification of a g=1.90 high-potenial iron-sulfur protein in chloroplasts. Biochem Biophys Res Comm 63: 1157–1160

    Article  PubMed  Google Scholar 

  • Mitchell P (1975) Protonmotive redox mechanism of the cytochrome bc 1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett 56: 1–6

    Article  PubMed  Google Scholar 

  • Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62: 327–367

    PubMed  Google Scholar 

  • 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: 9328–9337

    Google Scholar 

  • Prince RC, Lindsay JG and Dutton PL (1975) The Rieske iron-sulfur center in mitochondrial and photosynthetic systems: Em/pH relationships. FEBS Lett 51: 108–111

    Article  PubMed  Google Scholar 

  • Rich PR (1984) Electron and proton transfers through quinones and cytochrome bc complexes. Biochim Biophys Acta 768: 53–79

    PubMed  Google Scholar 

  • Rich PR (1986) A perspective on Q-cycles. J Bioenerg Biomembr 18: 145–156

    PubMed  Google Scholar 

  • Rieske JS (1976) Composition, structure and function of complex-III of the respiratory chain. Biochim Biophys Acta 456: 195–247

    PubMed  Google Scholar 

  • Rieske JS, Zaugg WS and Hansen RE (1964) Studies on the electron transfer system. LIX. Distribution of iron and of the component giving an electron paramagnetic resonance signal at g=1.90 in subfractions of complex III. J Biol Chem 239: 3017–3022

    PubMed  Google Scholar 

  • Saraste M (1984) Location of haem-binding sites in the mitochondrial cytochrome b. FEBS Lett 166: 367–372

    Article  PubMed  Google Scholar 

  • Schagger H, Borchant U, Machleidt W, Link TA and vonJagow G (1987) Isolation and amino acid sequence of the ‘Rieske’ iron-sulfur protein of beef heart ubiquinol-cytochrome c reductase. FEBS Lett 219: 161–168

    Article  PubMed  Google Scholar 

  • Simpkin D, Palmer G, Devlin FJ, Mckenna MC, Jensen GM and Stephens PJ (1989) The axial ligands of hemes in cytochromes: A near-Infrared magnetic circular dichroism study of yeast cytochromes c, c 1 and b and spinach cytochrome f. Biochemistry 28: 8033–8039

    PubMed  Google Scholar 

  • Steppuhn J, Rother C, Hermans J, Salnikow J, Hauska G and Herrmann RG (1987) The complete amino acid sequence of the Rieske Fe-S precursor protein from spinach chloroplasts deduced from cDNA analysis. Mol Gen Genet 210: 171–177

    Google Scholar 

  • Szczepaniak A and Cramer W (1990) Thylakoid membrane protein topography. Location of the termini of the chloroplast cytochrome b 6 on the stromal side of the membrane. J Biol Chem 265: 17720–17726

    PubMed  Google Scholar 

  • T'sai A-L and Palmer G (1983) Potentiometric studies of yeast complex III. Biochim Biophys Acta 722: 349–363

    PubMed  Google Scholar 

  • Telser J, Hoffmann BM, LoBrutto R, Ohnishi T, T'sai A-L, Simkin D and Palmer G (1987) Evidence for N coordination to Fe in the [2Fe-2S] center in yeast mitochondrial complex III. FEBS Lett 214: 117–121

    Article  PubMed  Google Scholar 

  • Thony-Meyer LD, Stax D and Hennecke H (1989) Discovery of an unusual gene cluster of the cytochrome bc 1 complex in Bradyrhizobium japonicum and its requirement for effective root nodule symbiosis. Cell 57: 683–697

    Article  PubMed  Google Scholar 

  • Trumpower B (1990) Cytochrome bc 1 complexes of microorganisms. Microbiol Revs 54: 101–129

    Google Scholar 

  • Trumpower BL and Katki AG (1979) Succinate-cytochrome c reductase complex of the mitochondrial electron transport chain. In: Capaldi RA (ed) Membrane Proteins in Energy Transduction, pp 89–200. Marcel Dekker, New York

    Google Scholar 

  • Trumpower BL, Edwards CA and Ohnishi T (1980) Reconstitution of the iron-sulfur protein responsible for the g=1.90 electron paramagnetic resonance signal and associated cytochrome c reductase activities to depleted succinate-cytochrome c reductase complex. J Biol Chem 255: 7487–7493

    PubMed  Google Scholar 

  • Widger WA, Cramer WA, Herrmann RG and Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the cytochrome b 6 f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81: 674–678

    PubMed  Google Scholar 

  • Widger WR (1991) The cloning of the Synechococcus PCC 7002 petCA operon: Implications on the cytochrome c 553 binding domain of cytochrome f. Photosyn Res 30: 71–84

    Google Scholar 

  • Willey DL and Gray JC (1988) Synthesis and assembly of the cytochrome bf complex in higher plants. Photosynth Res 17: 125–144

    Google Scholar 

  • Willey DL, Auffret AD and Gray JC (1984) Structure and topology of cytochrome f in pea chloroplast membranes. Cell 36: 555–562

    Article  PubMed  Google Scholar 

  • Wynn RM, Redlinger RE, Foster JM, Blankenship RE, Fuller RC, Shaw RW and Knaff DB (1987) Electron transport chains of phototrophically and chemotrophically grown Chloroflexus aurantiacus. Biochim Biophys Acta 891: 216–226

    Google Scholar 

  • Yang X and Trumpower B (1986) Purification of a three subunit ubiquinolcytochrome c oxidoreductase complex from Paracoccus denitrificans. J Biol Chem 261: 12282–12289

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Zannoni D and Ingledew WJ (1985) A thermodynamic analysis of the plasma membrane electron transport components in photoheterotrophically grown cells of Chloroflexus aurantiacus. FEBS Lett 193: 93–98

    Article  Google Scholar 

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Malkin, R. Cytochrome bc 1 and b 6 f complexes of photosynthetic membranes. Photosynth Res 33, 121–136 (1992). https://doi.org/10.1007/BF00039175

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