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. 1995 Feb;177(3):608–613. doi: 10.1128/jb.177.3.608-613.1995

Membrane-associated cytochrome cy of Rhodobacter capsulatus is an electron carrier from the cytochrome bc1 complex to the cytochrome c oxidase during respiration.

A Hochkoeppler 1, F E Jenney Jr 1, S E Lang 1, D Zannoni 1, F Daldal 1
PMCID: PMC176634  PMID: 7836293

Abstract

We have recently established that the facultative phototrophic bacterium Rhodobacter capsulatus has two different pathways for reduction of the photooxidized reaction center during photosynthesis (F.E. Jenney and F. Daldal, EMBO J. 12:1283-1292, 1993; F.E. Jenney, R.C. Prince, and F. Daldal, Biochemistry 33:2496-2502, 1994). One pathway is via the well-characterized, water-soluble cytochrome c2 (cyt c2), and the other is via a novel membrane-associated c-type cytochrome named cyt cy. In this work, we probed the role of cyt cy in respiratory electron transport by isolating a set of R. capsulatus mutants lacking either cyt c2 or cyt cy, in the presence or in the absence of a functional quinol oxidase-dependent alternate respiratory pathway. The growth and inhibitor sensitivity patterns of these mutants, their respiratory rates in the presence of specific inhibitors, and the oxidation-reduction kinetics of c-type cytochromes monitored under appropriate conditions demonstrated that cyt cy, like cyt c2, connects the bc1 complex and the cyt c oxidase during respiratory electron transport. Whether cyt c2 and cyt cy are the only electron carriers between these two energy-transducing membrane complexes of R. capsulatus is unknown.

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Selected References

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  1. Berry E. A., Trumpower B. L. Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc1 and cytochrome c-aa3 complexes. J Biol Chem. 1985 Feb 25;260(4):2458–2467. [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  3. Daldal F., Cheng S., Applebaum J., Davidson E., Prince R. C. Cytochrome c(2) is not essential for photosynthetic growth of Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2012–2016. doi: 10.1073/pnas.83.7.2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Daldal F. Cytochrome c2-independent respiratory growth of Rhodobacter capsulatus. J Bacteriol. 1988 May;170(5):2388–2391. doi: 10.1128/jb.170.5.2388-2391.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Daldal F., Davidson E., Cheng S. Isolation of the structural genes for the Rieske Fe-S protein, cytochrome b and cytochrome c1 all components of the ubiquinol: cytochrome c2 oxidoreductase complex of Rhodopseudomonas capsulata. J Mol Biol. 1987 May 5;195(1):1–12. doi: 10.1016/0022-2836(87)90322-6. [DOI] [PubMed] [Google Scholar]
  6. Daldal F., Tokito M. K., Davidson E., Faham M. Mutations conferring resistance to quinol oxidation (Qz) inhibitors of the cyt bc1 complex of Rhodobacter capsulatus. EMBO J. 1989 Dec 20;8(13):3951–3961. doi: 10.1002/j.1460-2075.1989.tb08578.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. García-Horsman J. A., Berry E., Shapleigh J. P., Alben J. O., Gennis R. B. A novel cytochrome c oxidase from Rhodobacter sphaeroides that lacks CuA. Biochemistry. 1994 Mar 15;33(10):3113–3119. doi: 10.1021/bi00176a046. [DOI] [PubMed] [Google Scholar]
  8. Gray K. A., Grooms M., Myllykallio H., Moomaw C., Slaughter C., Daldal F. Rhodobacter capsulatus contains a novel cb-type cytochrome c oxidase without a CuA center. Biochemistry. 1994 Mar 15;33(10):3120–3127. doi: 10.1021/bi00176a047. [DOI] [PubMed] [Google Scholar]
  9. Jenney F. E., Jr, Daldal F. A novel membrane-associated c-type cytochrome, cyt cy, can mediate the photosynthetic growth of Rhodobacter capsulatus and Rhodobacter sphaeroides. EMBO J. 1993 Apr;12(4):1283–1292. doi: 10.1002/j.1460-2075.1993.tb05773.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jenney F. E., Jr, Prince R. C., Daldal F. Roles of the soluble cytochrome c2 and membrane-associated cytochrome cy of Rhodobacter capsulatus in photosynthetic electron transfer. Biochemistry. 1994 Mar 8;33(9):2496–2502. doi: 10.1021/bi00175a019. [DOI] [PubMed] [Google Scholar]
  11. Jones M. R., McEwan A. G., Jackson J. B. The role of c-type cytochromes in the photosynthetic electron transport pathway of Rhodobacter capsulatus. Biochim Biophys Acta. 1990 Aug 9;1019(1):59–66. doi: 10.1016/0005-2728(90)90124-m. [DOI] [PubMed] [Google Scholar]
  12. Kutoh E., Sone N. Quinol-cytochrome c oxidoreductase from the thermophilic bacterium PS3. Purification and properties of a cytochrome bc1(b6f) complex. J Biol Chem. 1988 Jun 25;263(18):9020–9026. [PubMed] [Google Scholar]
  13. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  14. La Monica R. F., Marrs B. L. The branched respiratory system of photosynthetically grown Rhodopseudomonas capsulata. Biochim Biophys Acta. 1976 Mar 12;423(3):431–439. doi: 10.1016/0005-2728(76)90198-5. [DOI] [PubMed] [Google Scholar]
  15. Marrs B., Gest H. Genetic mutations affecting the respiratory electron-transport system of the photosynthetic bacterium Rhodopseudomonas capsulata. J Bacteriol. 1973 Jun;114(3):1045–1051. doi: 10.1128/jb.114.3.1045-1051.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Marrs B. Mobilization of the genes for photosynthesis from Rhodopseudomonas capsulata by a promiscuous plasmid. J Bacteriol. 1981 Jun;146(3):1003–1012. doi: 10.1128/jb.146.3.1003-1012.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Prince R. C., Baccarini-Melandri A., Hauska G. A., Melandri B. A., Crofts A. R. Asymmetry of an energy transducing membrane the location of cytochrome c2 in Rhodopseudomonas spheroides and Rhodopseudomonas capsulata. Biochim Biophys Acta. 1975 May 15;387(2):212–227. doi: 10.1016/0005-2728(75)90104-8. [DOI] [PubMed] [Google Scholar]
  18. Prince R. C., Daldal F. Physiological electron donors to the photochemical reaction center of Rhodobacter capsulatus. Biochim Biophys Acta. 1987 Dec 17;894(3):370–378. doi: 10.1016/0005-2728(87)90115-0. [DOI] [PubMed] [Google Scholar]
  19. Richardson D. J., McEwan A. G., Jackson J. B., Ferguson S. J. Electron transport pathways to nitrous oxide in Rhodobacter species. Eur J Biochem. 1989 Nov 20;185(3):659–669. doi: 10.1111/j.1432-1033.1989.tb15163.x. [DOI] [PubMed] [Google Scholar]
  20. Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [PubMed] [Google Scholar]
  21. Yen H. C., Hu N. T., Marrs B. L. Characterization of the gene transfer agent made by an overproducer mutant of Rhodopseudomonas capsulata. J Mol Biol. 1979 Jun 25;131(2):157–168. doi: 10.1016/0022-2836(79)90071-8. [DOI] [PubMed] [Google Scholar]
  22. Zannoni D., Baccarini-Melandri A., Malandri B. A. Energy transduction in photosynthetic bacteria. The nature of cytochrome C oxidase in the respiratory chain of Rhodopseudomonas capsulata. FEBS Lett. 1974 Nov 1;48(1):152–155. doi: 10.1016/0014-5793(74)81085-9. [DOI] [PubMed] [Google Scholar]
  23. Zannoni D., Daldal F. The role of c-type cytochromes in catalyzing oxidative and photosynthetic electron transport in the dual functional plasmamembrane of facultative phototrophs. Arch Microbiol. 1993;160(6):413–423. doi: 10.1007/BF00245301. [DOI] [PubMed] [Google Scholar]
  24. Zannoni D., Melandri B. A., Baccarini-Melandri A. Energy transduction in photosynthetic bacteria. X. Composition and function of the branched oxidase system in wild type and respiration deficient mutants of Rhodopseudomonas capsulata. Biochim Biophys Acta. 1976 Mar 12;423(3):413–430. doi: 10.1016/0005-2728(76)90197-3. [DOI] [PubMed] [Google Scholar]
  25. Zannoni D., Moore A. L. Measurement of the redox state of the ubiquinone pool in Rhodobacter capsulatus membrane fragments. FEBS Lett. 1990 Oct 1;271(1-2):123–127. doi: 10.1016/0014-5793(90)80387-x. [DOI] [PubMed] [Google Scholar]

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