Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Dec;177(23):6958–6965. doi: 10.1128/jb.177.23.6958-6965.1995

Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus.

J Buggy 1, C E Bauer 1
PMCID: PMC177566  PMID: 7592491

Abstract

The purple nonsulfur photosynthetic eubacterium Rhodobacter capsulatus is a versatile organism that can obtain cellular energy by several means, including the capture of light energy for photosynthesis as well as the use of light-independent respiration, in which molecular oxygen serves as a terminal electron acceptor. In this study, we have identified and characterized a novel gene, senC, mutations in which affect respiration as well as the induction of photosynthesis gene expression. The protein coded by senC exhibits 33% sequence identity to the yeast nucleus-encoded protein SCO1, which is thought to be a mitochondrion-associated cytochrome c oxidase assembly factor. Like yeast SCO1, SenC is required for optimal cytochrome c oxidase activity in aerobically grown R. capsulatus cells. We further show that senC is required for maximal induction from the puf and puh operons, which encode the structural polypeptides of the light-harvesting and reaction center complexes.

Full Text

The Full Text of this article is available as a PDF (295.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Au D. C., Lorence R. M., Gennis R. B. Isolation and characterization of an Escherichia coli mutant lacking the cytochrome o terminal oxidase. J Bacteriol. 1985 Jan;161(1):123–127. doi: 10.1128/jb.161.1.123-127.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baccarini-Melandri A., Jones O. T., Hauska G. Cytochrome c2--an electron carrier shared by the respiratory and photosynthetic electron transport chain of Rhodopseudomonas capsulata. FEBS Lett. 1978 Feb 15;86(2):151–154. doi: 10.1016/0014-5793(78)80551-1. [DOI] [PubMed] [Google Scholar]
  3. Bauer C. E., Buggy J. J., Yang Z. M., Marrs B. L. The superoperonal organization of genes for pigment biosynthesis and reaction center proteins is a conserved feature in Rhodobacter capsulatus: analysis of overlapping bchB and puhA transcripts. Mol Gen Genet. 1991 Sep;228(3):433–444. doi: 10.1007/BF00260637. [DOI] [PubMed] [Google Scholar]
  4. Bauer C. E., Young D. A., Marrs B. L. Analysis of the Rhodobacter capsulatus puf operon. Location of the oxygen-regulated promoter region and the identification of an additional puf-encoded gene. J Biol Chem. 1988 Apr 5;263(10):4820–4827. [PubMed] [Google Scholar]
  5. Bauer C., Buggy J., Mosley C. Control of photosystem genes in Rhodobacter capsulatus. Trends Genet. 1993 Feb;9(2):56–60. doi: 10.1016/0168-9525(93)90188-N. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Bruschi M., Guerlesquin F. Structure, function and evolution of bacterial ferredoxins. FEMS Microbiol Rev. 1988 Apr-Jun;4(2):155–175. doi: 10.1111/j.1574-6968.1988.tb02741.x. [DOI] [PubMed] [Google Scholar]
  8. Buchwald P., Krummeck G., Rödel G. Immunological identification of yeast SCO1 protein as a component of the inner mitochondrial membrane. Mol Gen Genet. 1991 Oct;229(3):413–420. doi: 10.1007/BF00267464. [DOI] [PubMed] [Google Scholar]
  9. Buggy J. J., Sganga M. W., Bauer C. E. Characterization of a light-responding trans-activator responsible for differentially controlling reaction center and light-harvesting-I gene expression in Rhodobacter capsulatus. J Bacteriol. 1994 Nov;176(22):6936–6943. doi: 10.1128/jb.176.22.6936-6943.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Buggy J. J., Sganga M. W., Bauer C. E. Nucleotide sequence and characterization of the Rhodobacter capsulatus hvrB gene: HvrB is an activator of S-adenosyl-L-homocysteine hydrolase expression and is a member of the LysR family. J Bacteriol. 1994 Jan;176(1):61–69. doi: 10.1128/jb.176.1.61-69.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cooper C. E., Nicholls P., Freedman J. A. Cytochrome c oxidase: structure, function, and membrane topology of the polypeptide subunits. Biochem Cell Biol. 1991 Sep;69(9):586–607. doi: 10.1139/o91-089. [DOI] [PubMed] [Google Scholar]
  12. Costanzo M. C., Fox T. D. Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu Rev Genet. 1990;24:91–113. doi: 10.1146/annurev.ge.24.120190.000515. [DOI] [PubMed] [Google Scholar]
  13. Cuypers H., Zumft W. G. Anaerobic control of denitrification in Pseudomonas stutzeri escapes mutagenesis of an fnr-like gene. J Bacteriol. 1993 Nov;175(22):7236–7246. doi: 10.1128/jb.175.22.7236-7246.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Eraso J. M., Kaplan S. Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides: a mutant histidine kinase. J Bacteriol. 1995 May;177(10):2695–2706. doi: 10.1128/jb.177.10.2695-2706.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. García-Horsman J. A., Barquera B., Rumbley J., Ma J., Gennis R. B. The superfamily of heme-copper respiratory oxidases. J Bacteriol. 1994 Sep;176(18):5587–5600. doi: 10.1128/jb.176.18.5587-5600.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Green G. N., Gennis R. B. Isolation and characterization of an Escherichia coli mutant lacking cytochrome d terminal oxidase. J Bacteriol. 1983 Jun;154(3):1269–1275. doi: 10.1128/jb.154.3.1269-1275.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Grossman A. D. Integration of developmental signals and the initiation of sporulation in B. subtilis. Cell. 1991 Apr 5;65(1):5–8. doi: 10.1016/0092-8674(91)90353-z. [DOI] [PubMed] [Google Scholar]
  20. Hartl F. U., Pfanner N., Nicholson D. W., Neupert W. Mitochondrial protein import. Biochim Biophys Acta. 1989 Jan 18;988(1):1–45. doi: 10.1016/0304-4157(89)90002-6. [DOI] [PubMed] [Google Scholar]
  21. Hochkoeppler A., Jenney F. E., Jr, Lang S. E., Zannoni D., Daldal F. Membrane-associated cytochrome cy of Rhodobacter capsulatus is an electron carrier from the cytochrome bc1 complex to the cytochrome c oxidase during respiration. J Bacteriol. 1995 Feb;177(3):608–613. doi: 10.1128/jb.177.3.608-613.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hüdig H., Drews G. Characterization of a new membrane-bound cytochrome c of Rhodopseudomonas capsulata. FEBS Lett. 1983 Feb 21;152(2):251–255. doi: 10.1016/0014-5793(83)80390-1. [DOI] [PubMed] [Google Scholar]
  23. Inoue K., Kouadio J. L., Mosley C. S., Bauer C. E. Isolation and in vitro phosphorylation of sensory transduction components controlling anaerobic induction of light harvesting and reaction center gene expression in Rhodobacter capsulatus. Biochemistry. 1995 Jan 17;34(2):391–396. doi: 10.1021/bi00002a002. [DOI] [PubMed] [Google Scholar]
  24. Krummeck G., Rödel G. Yeast SCO1 protein is required for a post-translational step in the accumulation of mitochondrial cytochrome c oxidase subunits I and II. Curr Genet. 1990 Jul;18(1):13–15. doi: 10.1007/BF00321109. [DOI] [PubMed] [Google Scholar]
  25. Kuhn-Nentwig L., Kadenbach B. Isolation and properties of cytochrome c oxidase from rat liver and quantification of immunological differences between isozymes from various rat tissues with subunit-specific antisera. Eur J Biochem. 1985 May 15;149(1):147–158. doi: 10.1111/j.1432-1033.1985.tb08905.x. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Lampe H. H., Drews G. Die Differenzierung des Membransystems von Rhodopseudomonas capsulata hinsichtlich seiner photosynthetischen und respiratorischen Funktionen. Arch Mikrobiol. 1972;84(1):1–19. [PubMed] [Google Scholar]
  28. 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]
  29. Minghetti K. C., Goswitz V. C., Gabriel N. E., Hill J. J., Barassi C. A., Georgiou C. D., Chan S. I., Gennis R. B. Modified, large-scale purification of the cytochrome o complex (bo-type oxidase) of Escherichia coli yields a two heme/one copper terminal oxidase with high specific activity. Biochemistry. 1992 Aug 4;31(30):6917–6924. doi: 10.1021/bi00145a008. [DOI] [PubMed] [Google Scholar]
  30. Mosley C. S., Suzuki J. Y., Bauer C. E. Identification and molecular genetic characterization of a sensor kinase responsible for coordinately regulating light harvesting and reaction center gene expression in response to anaerobiosis. J Bacteriol. 1994 Dec;176(24):7566–7573. doi: 10.1128/jb.176.24.7566-7573.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nossal G. J. The molecular and cellular basis of affinity maturation in the antibody response. Cell. 1992 Jan 10;68(1):1–2. doi: 10.1016/0092-8674(92)90198-l. [DOI] [PubMed] [Google Scholar]
  32. Ohlsen K. L., Grimsley J. K., Hoch J. A. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1756–1760. doi: 10.1073/pnas.91.5.1756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Perego M., Hanstein C., Welsh K. M., Djavakhishvili T., Glaser P., Hoch J. A. Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell. 1994 Dec 16;79(6):1047–1055. doi: 10.1016/0092-8674(94)90035-3. [DOI] [PubMed] [Google Scholar]
  34. Prentki P., Krisch H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. doi: 10.1016/0378-1119(84)90059-3. [DOI] [PubMed] [Google Scholar]
  35. Scherer S. Do photosynthetic and respiratory electron transport chains share redox proteins? Trends Biochem Sci. 1990 Dec;15(12):458–462. doi: 10.1016/0968-0004(90)90296-n. [DOI] [PubMed] [Google Scholar]
  36. Schulze M., Rödel G. Accumulation of the cytochrome c oxidase subunits I and II in yeast requires a mitochondrial membrane-associated protein, encoded by the nuclear SCO1 gene. Mol Gen Genet. 1989 Mar;216(1):37–43. doi: 10.1007/BF00332228. [DOI] [PubMed] [Google Scholar]
  37. Schulze M., Rödel G. SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II. Mol Gen Genet. 1988 Mar;211(3):492–498. doi: 10.1007/BF00425706. [DOI] [PubMed] [Google Scholar]
  38. Smits P. H., De Haan M., Maat C., Grivell L. A. The complete sequence of a 33 kb fragment on the right arm of chromosome II from Saccharomyces cerevisiae reveals 16 open reading frames, including ten new open reading frames, five previously identified genes and a homologue of the SCO1 gene. Yeast. 1994 Apr;10 (Suppl A):S75–S80. doi: 10.1002/yea.320100010. [DOI] [PubMed] [Google Scholar]
  39. Taanman J. W., Capaldi R. A. Purification of yeast cytochrome c oxidase with a subunit composition resembling the mammalian enzyme. J Biol Chem. 1992 Nov 5;267(31):22481–22485. [PubMed] [Google Scholar]
  40. Trumpower B. L. Cytochrome bc1 complexes of microorganisms. Microbiol Rev. 1990 Jun;54(2):101–129. doi: 10.1128/mr.54.2.101-129.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tzagoloff A., Capitanio N., Nobrega M. P., Gatti D. Cytochrome oxidase assembly in yeast requires the product of COX11, a homolog of the P. denitrificans protein encoded by ORF3. EMBO J. 1990 Sep;9(9):2759–2764. doi: 10.1002/j.1460-2075.1990.tb07463.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tzagoloff A., Dieckmann C. L. PET genes of Saccharomyces cerevisiae. Microbiol Rev. 1990 Sep;54(3):211–225. doi: 10.1128/mr.54.3.211-225.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Visser E. S., McGuire T. C., Palmer G. H., Davis W. C., Shkap V., Pipano E., Knowles D. P., Jr The Anaplasma marginale msp5 gene encodes a 19-kilodalton protein conserved in all recognized Anaplasma species. Infect Immun. 1992 Dec;60(12):5139–5144. doi: 10.1128/iai.60.12.5139-5144.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Weaver P. F., Wall J. D., Gest H. Characterization of Rhodopseudomonas capsulata. Arch Microbiol. 1975 Nov 7;105(3):207–216. doi: 10.1007/BF00447139. [DOI] [PubMed] [Google Scholar]
  45. Wellington C. L., Taggart A. K., Beatty J. T. Functional significance of overlapping transcripts of crtEF, bchCA, and puf photosynthesis gene operons in Rhodobacter capsulatus. J Bacteriol. 1991 May;173(9):2954–2961. doi: 10.1128/jb.173.9.2954-2961.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Young D. A., Bauer C. E., Williams J. C., Marrs B. L. Genetic evidence for superoperonal organization of genes for photosynthetic pigments and pigment-binding proteins in Rhodobacter capsulatus. Mol Gen Genet. 1989 Jul;218(1):1–12. doi: 10.1007/BF00330558. [DOI] [PubMed] [Google Scholar]
  47. Zannoni D., Jasper P., Marrs B. Light-induced oxygen reduction as a probe of electron transport between respiratory and photosynthetic components in membranes of Rhodopseudomonas capsulata. Arch Biochem Biophys. 1978 Dec;191(2):625–631. doi: 10.1016/0003-9861(78)90400-9. [DOI] [PubMed] [Google Scholar]
  48. Zannoni D., Melandri B. A., Baccarini-Melandri A. Energy tranduction in photosynthetic bacteria. XI. Further resolution of cytochromes of b type and the nature of the co-sensitive oxidase present in the respiratory chain of Rhodopseudomonas capsulata. Biochim Biophys Acta. 1976 Dec 6;449(3):386–400. doi: 10.1016/0005-2728(76)90150-x. [DOI] [PubMed] [Google Scholar]
  49. 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]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES