Abstract
The cytochromeb/c 1 complex is an ubiquitous energy transducing enzyme, part of the electron transport chain of prokaryotes, mitochondria, and chloroplasts (b 6/f). In the ancient purple photosynthetic bacteria, theb/c 1 complex occupies a central metabolic role, being part of their photosynthetic and respiratory electron transport chain. InRhodobacter the three subunits of theb/c 1 complex are FeS protein, cytochromeb, and cytochromec 1, and they are encoded by a constitutively expressed operon namedfbc. The organization of the genes for the cytochromeb/c 1 complex, the modality of transcription, and the biogenesis of the encoded polypeptides will be described. TheRhodobacter species used to isolate thefbc genes, previously reported asR. sphaeroides was identified asR. capsulatus. Further biochemical characterization of the prokaryoticb/c 1 complex indicated that the three polypeptides encoded by thefbc operon comprise the entire catalytic structure: ubiquinol-cytochrome-c reductase.
The amino acid sequences of the threeb/c 1 subunits from the photosynthetic bacteriumRhodobacter capsulatus were compared with the corresponding sequences from yeast mitochondria and spinach chloroplasts. The high homology found between the sequences of all three redox polypeptides fromR. capsulatus and yeast mitochondria (cytochromeb 41%, FeS protein 46%, cytochromec 1 31%) provided further evidence that mitochondria arose from the phylogenetic line of purple bacteria. The structure of cytochromeb also exhibited considerable homology to chloroplast cytochromeb 6 plus subunit IV (26%). The amino acid sequence of the Rieske FeS protein fromR. capsulatus and chloroplasts were found to be conserved only in the C-terminal part (14% total identity), whereas the homology between cytochromec 1 and cytochromef is very weak (12%), despite similar topology of the two polypeptides.
Analysis of the homology suggested that the catalytic sites quinol oxidase (Qo) and quinone reductase (Qi) arose monophonetically, whereas cytochromec and plastocyanin reductase sites are not homologous and could derive from diverse ancestral genes by convergent evolution.
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Abbreviations
- kb:
-
kilobase
- kDa:
-
kilodalton
- SDS-PAGE:
-
sodium dodecyl sulfate polyacrylamide gel electrophoresis
References
Alt, J., and Herrmann, G. (1984).Curr. Genet. 8, 551–557
Alt, J., Westhoff, P., Sears, B. B., Nelson, N., Hurt, E., Hauska, G., and Herrmann, R. G. (1983).EMBO J. 2, 979–986.
Avtges, P., Scolnik, P. A., and Haselkorn, R. (1983).J. Bacteriol. 156, 251–256.
Baccarini-Melandri, A., and Zannoni, D. (1978).J. Bioenerg. Biomembr. 10, 109–138.
Baccarini-Melandri, A., Gabellini, N., and Melandri, B. A., Jones, K. R., Rutherford, A. W., Crofts, A. R., and Hurt, E. (1982).Arch. Biochem. Biophys. 216, 566–580.
Bartsch, R. G. (1971).Methods Enzymol. 23, 344–363.
Beckmann, J. D., Ljungdahl, P. O., Lopez, J. L., and Trumpower, B. L. (1987).J. Biol. Chem. 262, 8901–8909.
Chang, C. H., Tiede, D., Tang, J., Smith, U., Norris, J., and Schiffer, M. (1986).FEBS Lett. 205, 82–86.
Chory, J., and Kaplan, S. (1982).J. Biol. Chem. 257, 15110–15121.
Colson, A. M., and Slonimski, P. P. (1979).Mol. Gen. Genet. 167, 287–298.
Crofts, A. R. (1987). InCytochrome Systems: Molecular Biology and Bioenergetics (Papa, S., ed.), Plenum Press, New York, in press.
Crofts, A. R., Meinhardt, S. W., Jones, K. R., and Snozzi, M. (1983).Biochim. Biophys. Acta 723, 202–218.
Davidson, E., and Daldal, F. (1987a).J. Mol. Biol. 195, 13–24.
Davidson, E., and Daldal, F. (1987b).J. Mol. Biol. 195, 25–29.
Diesenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985).Nature (London)318, 618–624.
Dickerson, R. E., and Timkovich, R. (1975). InThe Enzyme, (Boyer, P. D., ed.), Academic Press, New York, Vol. 11, pp. 397–547.
Falk, G., Hampe, A., and Walker, E. J. (1985).Biochem. J. 228, 391–407.
Fee, J. A., Findling, K. L., Yoshida, T., Hille, R., Tarr, G. E., Hearshen, D. O., Dunham, W. R., Day, E. P., Kent, T. A., and Münck, E. (1984).J. Biol. Chem. 259, 124–133.
Fox, G. E., Stackebrandt, E., Hespell, R. B., Gibson, J., Maniloff, J., Dyer, T. A., Wolfe, R. S., Balch, W. E., Tanner, R. S., Magrum, L. J., Zablen, L. B., Blankemore, R., Gupta, R., Bonen, L., Lewis, B. J., Stahl, D. A., Luehrsen, K. R., Chen, K. N., and Woese, C. R. (1980).Science 209, 457–463.
Gabellini, N., and Hauska, G. (1983).FEBS Lett. 154, 171–174.
Gabellini, N., and Sebald, W. (1986).Eur. J. Biochem. 154, 569–579.
Gabellini, N., Bowyer, J. R., Hurt, E., Melandri, B. A., and Hauska, G. (1982).Eur. J. Biochem. 126, 105–111.
Gabellini, N., Harnish, U., McCarthy, J. E. G., Hauska, G., and Sebald, W. (1985).EMBO J. 4, 549–553.
Gibson, F. (1982).Proc. R. Soc. London Ser. B 251, 1–18.
Gibson, J., Stackebrandt, E., Zablen, L., Gupta, R., and Woese, C. R. (1979).Curr. Microbiol. 3, 59–64.
Hallick, R. B., and Bottomley, W. (1983).Plant. Mol. Biol. Rep. 1, 38–45.
Harnisch, U., Weiss, H., and Sebald, W. (1985).Eur. J. Biochem. 149, 95–99.
Hartl, F. U., Schmidt, B., Wachter, E., Weiss, H., and Neupert, W. (1986).Cell 47, 939–951.
Hauska, G., Hurt, E., Gabellini, N., and Lokau, W. (1983).Biochim. Biophys. Acta 726, 97–133.
Hauska, G., Nitsche, W., and Herrmann, R. G. (1988).J. Bioenerg. Biomembr., submitted.
Heinemayer, W., Alt, G., and Herrmann, R. G. (1984).Curr. Genet. 8, 543–549.
Hurt, E., and Hauska, G. (1981).Eur. J. Biochem. 117, 591–559.
Imhoff, J. F., Trüper, H. G., and Pfennig, N. (1984).Int. J. Sist. Bacteriol. 34, 340–343.
Kallas, T., Spiller, S., and Malkin, R. (1986). Abstracts VII Int. Congress on Photosynthesis, Brown University, Providence, Rhode Island.
Kurowski, B., and Ludwig, B. (1987).J. Biol. Chem. 262, 13805–13811.
Link, T. A., Schägger, H., and von Jagow, G. (1986)FEBS Lett. 204, 9–15.
McClure, W. R. (1985).Annu. Rev. Biochem. 54, 171–204.
Michaelis, S., and Beckwith, J. (1982).Annu. Rev. Microbiol. 36, 435–465.
Mitchell, P. (1976).J. Theor. Biol. 62, 327–367.
Niederman, R. A., and Gibson, K. D. (1978). InThe Photosynthetic Bacteria (Clayton, R. K., and Sistrom, W. R., eds.), Plenum Press, New York, pp. 79–113.
Nobrega, F. G., and Tzagoloff, A. (1980).J. Biol. Chem. 255, 9828–9837.
Okamura, M. Y., Feher, G., and Nelson, N. (1982). InPhotosynthesis (Govindjee, ed.), Academic Press, New York, pp. 195–272.
Oesterhelt, D., and Stoeckenius, W., (1973).Proc. Natl. Acad. Sci. U.S.A. 70, 2853–2857.
Paetow, B., and Ludwig, B. (1986). Fourth EBEC, Short Reports, p. 102, Prague.
Paetow, B., Ferguson, S., Gabellini, N., Hoeren, F., Ludwig, B., and McCarthy, J. E. G. (1986). Fourth EBEC, Short Reports, p. 101, Prague.
Platt, T. (1981).Cell 24, 10–23.
Pfennig, N. (1978). InThe Photosynthetic Bacteria (Clayton, R. K., and Sistrom, W. R., eds.), Plenum Press, New York, pp. 3–18.
Rapoport, T. A., and Wiedmann, M. (1985).Curr. Top. Membr. Transp. 24, 1–61.
Rieske, J. S., MacLennan, D. H., and Coleman, R. (1964).Biochem. Biophys. Res. Commun. 15, 338–344.
Robertson, D. E., Davidson, E., Prince, R. C., van den Berg, W. H., Marrs, B. L., and Dutton, P. L. (1986).J. Biol. Chem. 261, 584–591.
Sadler, I., Suda, K., Schatz, G., Kaudewitz, F., and Haid, A. (1984).EMBO J. 3, 2137–2143.
Saraste, M. (1984).FEBS Lett. 166, 367–372.
Shine, J., and Dalgarno, K. (1975).Nature (London)254, 34–38.
Sistrom, W. R. (1978). InThe Photosynthetic Bacteria (Clayton, R. K., and Sistrom, W. R., eds.), Plenum Press, New York, pp. 927–934.
Steppuhn, J., Hermans, J., Janson, T., Vater, J., Hauska, J., and Herrmann, R. G. (1987).Mol. Gen. Genet., in press.
Stout, C. D. (1982). InIron-Sulfur Proteins (Spiro, T. G., ed.), Wiley, New York, pp. 97–146.
Telser, J., Hoffman, B. M., LoBrutto, R., Ohnishi, T., Tsai, A. L., Simpkin, D., and Palmer, G. (1987).FEBS Lett. 214, 117–121.
Tybulewicz, V. L. J., Falk, G., and Walker, J. E. (1984).J. Mol. Biol. 179, 185–214.
Von Jagow, G., and Sebald, W. (1980).Annu. Rev. Biochem. 49, 281–314.
Wakabayashi, S., Matsubara, H., Kim, C. H., Kawai, K., and King, E. (1980).Biochem. Biophys. Res. Commun. 97, 1548–1554.
Wakabayashi, S., Takeda, H., Matsubara, H., Kim, C. H., and King, T. E. (1982).J. Biochem. 91, 2077–2085.
Weaver, P. F., Wall, J. D., and Gest, H. (1975).Arch. Microbiol. 105, 207–216.
Weyer, K. A., Lottspeich, F., Gruenberg, H., Lang, F., Oesterhelt, D., and Michel, H. (1987).EMBO J. 8, 2197–2202.
Widger, W. R., Cramer, W. A., Herrmann, R. G., and Trebst, A. (1984).Proc. Natl. Acad. Sci. USA 81, 674–678.
Willey, D. L., Howe, C. J., Auffret, A. D., Bowman, C. M., Dyer, T. A., and Gray, J. C. (1984).Mol. Gen. Genet. 194, 416–422.
Williams, J. C., Steiner, L. A., Feher, G., and Simon, M. I. (1984).Proc. Natl. Acad. Sci. USA 81, 7303–7307.
Wilson, E., Farley, T. M., and Takemoto, J. Y., (1985).J. Biol. Chem. 260, 10288–10292.
Woese, C. R., Stackebrandt, E., Weisburg, W. G., Paster, B. J., Madigan, M. T., Fowler, V. J., Hahn, C. M., Blanz, P., Gupt, R., Nealson, K. H., and Fox, G. E. (1984).Syst. Appl. Microbiol. 5, 315–326.
Wynn, R. M., Gaul, D. F., Choi, W. K., Shaw, R. W., and Knaff, D. B. (1986).Photosynth. Res. 9 181–195.
Yang, X., and Trumpower, B. L. (1986).J. Biol. Chem. 261, 12282–12289.
Youvan, D., Bylina, E. J., Albert, M., Begusch, H., and Hearst, J. E. (1984).Cell 34, 949–957.
Yu, C. A., and Yu, L. (1981).Biochim. Biophys. Acta 639, 99–128.
Yu, L., and Yu, C. A. (1982).Biochem. Biophys. Commun. 108, 1285–1292.
Zannoni, D., and Marrs, B. (1981).Biochim. Biophys. Acta 637, 96–106.
Zsebo, K. M., and Hearst, J. E. (1984).Cell 37, 937–947.
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Gabellini, N. Organization and structure of the genes for the cytochromeb/c 1 complex in purple photosynthetic bacteria. A phylogenetic study describing the homology of theb/c 1 subunits between prokaryotes, mitochondria, and chloroplasts. J Bioenerg Biomembr 20, 59–83 (1988). https://doi.org/10.1007/BF00762138
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DOI: https://doi.org/10.1007/BF00762138