1887

Abstract

Using transposon mutagenesis, mutations have been isolated in several genes ( and ) that play a role in cytochrome metabolism. As in other bacteria, mutations in the and genes resulted in the absence of all -type cytochromes. However, the mutant also lacked cytochrome oxidase , a defect that does not appear to have been reported for other bacteria. The -type cytochromes were also missing from a mutant strain with an insertion into the gene encoding the haem-containing subunit (SU)I of cytochrome oxidase, but not in mutants unable to make SUII or SUIII, indicating that CcdA probably plays a role in assembling SUI. The cytochrome-deficient mutants also had other free-living phenotypes, including a significant decrease in growth rate on rich media and increased motility on minimal media. A mutant also had significantly decreased motility, but the motility and growth properties of the mutant were unchanged. Unlike similar mutants in and , an Rm1021 mutant contained cytochrome oxidase . Cytochrome maturation in strain Rm1021 appeared to be similar to maturation in other rhizobia, but there were some differences in the cytochrome composition of the strain, and respiration chain function and assembly.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/002634-0
2007-02-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/399.html?itemId=/content/journal/micro/10.1099/mic.0.2006/002634-0&mimeType=html&fmt=ahah

References

  1. Aguilar, G. R. & Soberon, M. ( 1996; ). Cloning and sequence analysis of the Rhizobium etli ccmA and ccmB genes involved in c-type cytochrome biogenesis. Gene 182, 129–135.[CrossRef]
    [Google Scholar]
  2. Bardischewsky, F. & Friedrich, C. G. ( 2001; ). Identification of ccdA in Paracoccus pantotrophus GB17: disruption of ccdA causes complete deficiency in c-type cytochromes. J Bacteriol 183, 257–263.[CrossRef]
    [Google Scholar]
  3. Beckett, C. S., Loughman, J. A., Karberg, K. A., Donato, G. M., Goldman, W. E. & Kranz, R. G. ( 2000; ). Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis, a unique bacterial model. Mol Microbiol 38, 465–481.[CrossRef]
    [Google Scholar]
  4. Bott, M., Ritz, D. & Hennecke, H. ( 1991; ). The Bradyrhizobium japonicum cycM gene encodes a membrane-anchored homolog of mitochondrial cytochrome c. J Bacteriol 173, 6766–6772.
    [Google Scholar]
  5. Buggy, J. & Bauer, C. E. ( 1995; ). Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus. J Bacteriol 177, 6958–6965.
    [Google Scholar]
  6. Cianciotto, N. P., Cornelis, P. & Baysse, C. ( 2005; ). Impact of the bacterial type I cytochrome c maturation system on different biological processes. Mol Microbiol 56, 1408–1415.[CrossRef]
    [Google Scholar]
  7. Cinege, G., Kereszt, A., Kertesz, S., Balogh, G. & Dusha, I. ( 2004; ). The roles of different regions of the CycH protein in c-type cytochrome biogenesis in Sinorhizobium meliloti. Mol Genet Genomics 271, 171–179.[CrossRef]
    [Google Scholar]
  8. Delgado, M. J., Yeoman, K. H., Wu, G., Vargas, C., Davies, A. E., Poole, R. K., Johnston, A. W. & Downie, J. A. ( 1995; ). Characterization of the cycHJKL genes involved in cytochrome c biogenesis and symbiotic nitrogen fixation in Rhizobium leguminosarum. J Bacteriol 177, 4927–4934.
    [Google Scholar]
  9. Delgado, M. J., Bedmar, E. J. & Downie, A. J. ( 1998; ). Genes involved in the formation and assembly of rhizobial cytochromes and their role in symbiotic nitrogen fixation. Adv Microb Physiol 40, 192–203.
    [Google Scholar]
  10. Deshmukh, M., Brasseur, G. & Daldal, F. ( 2000; ). Novel Rhodobacter capsulatus genes required for the biogenesis of various c-type cytochromes. Mol Microbiol 35, 123–138.[CrossRef]
    [Google Scholar]
  11. Djordjevic, M. A., Chen, H. C., Natera, S., Van Noorden, G., Menzel, C., Taylor, S., Renard, C., Geiger, O. & Weiller, G. F.; Sinorhizobium DNA Sequencing Consortium ( 2003; ). A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation. Mol Plant Microbe Interact 16, 508–524.[CrossRef]
    [Google Scholar]
  12. Feissner, R., Xiang, Y. & Kranz, R. G. ( 2003; ). Chemiluminescent-based methods to detect subpicomole levels of c-type cytochromes. Anal Biochem 315, 90–94.[CrossRef]
    [Google Scholar]
  13. Finan, T. M., Hartweig, E., LeMieux, K., Bergman, K., Walker, G. C. & Signer, E. R. ( 1984; ). General transduction in Rhizobium meliloti. J Bacteriol 159, 120–124.
    [Google Scholar]
  14. Galibert, F., Finan, T. M., Long, S. R., Pühler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A. & other authors ( 2001; ). The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668–672.[CrossRef]
    [Google Scholar]
  15. Glerum, D. M., Shtanko, A. & Tzagoloff, A. ( 1996; ). SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J Biol Chem 271, 20531–20535.[CrossRef]
    [Google Scholar]
  16. Hamel, P. P., Dreyfuss, B. W., Xie, Z., Gabilly, S. T. & Merchant, S. ( 2003; ). Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J Biol Chem 278, 2593–2603.[CrossRef]
    [Google Scholar]
  17. Huang, H. C., He, S., Bauer, Y. D. W. & Collmer, A. ( 1992; ). The Pseudomonas syringae pv. syringae 61 hrpH product, an envelope protein required for elicitation of the hypersensitive response in plants. J Bacteriol 174, 6878–6885.
    [Google Scholar]
  18. Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. ( 1995; ). Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660–669.[CrossRef]
    [Google Scholar]
  19. Kadokura, H., Katzen, F. & Beckwith, J. ( 2003; ). Protein disulfide bond formation in prokaryotes. Annu Rev Biochem 72, 111–135.[CrossRef]
    [Google Scholar]
  20. Kereszt, A., Slaska-Kiss, K., Putnoky, P., Banfalvi, Z. & Kondorosi, A. ( 1995; ). The cycHJKL genes of Rhizobium meliloti involved in cytochrome c biogenesis are required for “respiratory” nitrate reduction ex planta and for nitrogen fixation during symbiosis. Mol Gen Genet 247, 39–47.[CrossRef]
    [Google Scholar]
  21. Kimball, R. A., Martin, L. & Saier, M. H., Jr ( 2003; ). Reversing transmembrane electron flow: the DsbD and DsbB protein families. J Mol Microbiol Biotechnol 5, 133–149.[CrossRef]
    [Google Scholar]
  22. Knobloch, J. K., Nedelmann, M., Kiel, K., Bartscht, K., Horstkotte, M. A., Dobinsky, S., Rohde, H. & Mack, D. ( 2003; ). Establishment of an arbitrary PCR for rapid identification of Tn917 insertion sites in Staphylococcus epidermidis: characterization of biofilm-negative and nonmucoid mutants. Appl Environ Microbiol 69, 5812–5818.[CrossRef]
    [Google Scholar]
  23. Kranz, R. G., Beckett, C. S. & Goldman, B. S. ( 2002; ). Genomic analyses of bacterial respiratory and cytochrome c assembly systems: Bordetella as a model for the system II cytochrome c biogenesis pathway. Res Microbiol 153, 1–6.[CrossRef]
    [Google Scholar]
  24. Leary, S. C., Kaufman, B. A., Pellecchia, G., Guercin, G. H., Mattman, A., Jaksch, M. & Shoubridge, E. A. ( 2004; ). Human SCO1 and SCO2 have independent, cooperative functions in copper delivery to cytochrome c oxidase. Hum Mol Genet 13, 1839–1848.[CrossRef]
    [Google Scholar]
  25. Le Brun, N. E., Bengtsson, J. & Hederstedt, L. ( 2000; ). Genes required for cytochrome c synthesis in Bacillus subtilis. Mol Microbiol 36, 638–650.
    [Google Scholar]
  26. Marroqui, S., Zorreguieta, A., Santamaria, C., Temprano, F., Soberon, M., Megias, M. & Downie, J. A. ( 2001; ). Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. J Bacteriol 183, 854–864.[CrossRef]
    [Google Scholar]
  27. Marrs, B. & Gest, H. ( 1973; ). Genetic mutations affecting the respiratory electron-transport system of the photosynthetic bacterium Rhodopseudomonas capsulata. J Bacteriol 114, 1045–1051.
    [Google Scholar]
  28. McDermott, T. R. & Kahn, M. L. ( 1992; ). Cloning and mutagenesis of the Rhizobium meliloti isocitrate dehydrogenase gene. J Bacteriol 174, 4790–4797.
    [Google Scholar]
  29. O'Brian, M. R. & Maier, R. J. ( 1989; ). Molecular aspects of the energetics of nitrogen fixation in Rhizobium-legume symbioses. Biochim Biophys Acta 974, 229–246.[CrossRef]
    [Google Scholar]
  30. O'Brian, M. R. & Thony-Meyer, L. ( 2002; ). Biochemistry, regulation and genomics of haem biosynthesis in prokaryotes. Adv Microb Physiol 46, 257–318.
    [Google Scholar]
  31. Oh, J. I., Ko, I. J. & Kaplan, S. ( 2004; ). Reconstitution of the Rhodobacter sphaeroides cbb 3-PrrBA signal transduction pathway in vitro. Biochemistry 43, 7915–7923.[CrossRef]
    [Google Scholar]
  32. Ortenberg, R. & Beckwith, J. ( 2003; ). Functions of thiol-disulfide oxidoreductases in E. coli: redox myths, realities, and practicalities. Antioxid Redox Signal 5, 403–411.[CrossRef]
    [Google Scholar]
  33. Page, M. D. & Ferguson, S. J. ( 1999; ). Mutational analysis of the Paracoccus denitrificans c-type cytochrome biosynthetic genes ccmABCDG: disruption of ccmC has distinct effects suggesting a role for CcmC independent of CcmAB. Microbiology 145, 3047–3057.
    [Google Scholar]
  34. Poole, R. K. ( 1994; ). Oxygen reaction with bacterial oxidases and globins: binding, reduction and regulation. Antonie van Leeuwenhoek 65, 289–310.[CrossRef]
    [Google Scholar]
  35. Ramseier, T. M., Kaluza, B., Studer, D., Gloudemans, T., Bisseling, R., Jordan, M. P., Jones, R. M., Zuber, M. & Hennecke, H. ( 1989; ). Cloning of a DNA region from Bradyrhizobium japonicum encoding pleiotropic functions in heme metabolism and respiration. Arch Microbiol 151, 203–212.[CrossRef]
    [Google Scholar]
  36. Ramseier, T. M., Winteler, H. V. & Hennecke, H. ( 1991; ). Discovery and sequence analysis of bacterial genes involved in the biogenesis of c-type cytochromes. J Biol Chem 266, 7793–7803.
    [Google Scholar]
  37. Renalier, M. H., Batut, J., Ghai, J., Terzaghi, B., Gherardi, M., David, M., Garnerone, A. M., Vasse, J., Truchet, G. & other authors ( 1987; ). A new symbiotic cluster on the pSym megaplasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J Bacteriol 169, 2231–2238.
    [Google Scholar]
  38. Reyes, J. D., Tabche, M., Morera, C., Girard, M. L., Romero, D., Krol, E., Miranda, J. & Soberon, M. ( 2000; ). Expression pattern of Rhizobium etli ccmIEFH genes involved in c-type cytochrome maturation. Gene 250, 149–157.[CrossRef]
    [Google Scholar]
  39. Ritz, D., Bott, M. & Hennecke, H. ( 1993; ). Formation of several bacterial c-type cytochromes requires a novel membrane-anchored protein that faces the periplasm. Mol Microbiol 9, 729–740.[CrossRef]
    [Google Scholar]
  40. Ritz, D., Thony-Meyer, L. & Hennecke, H. ( 1995; ). The cycHJKL gene cluster plays an essential role in the biogenesis of c-type cytochromes in Bradyrhizobium japonicum. Mol Gen Genet 247, 27–38.[CrossRef]
    [Google Scholar]
  41. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. & Puhler, A. ( 1994; ). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69–73.[CrossRef]
    [Google Scholar]
  43. Schulz, H. & Thony-Meyer, L. ( 2000; ). Interspecies complementation of Escherichia coli ccm mutants: CcmE (CycJ) from Bradyrhizobium japonicum acts as a heme chaperone during cytochrome c maturation. J Bacteriol 182, 6831–6833.[CrossRef]
    [Google Scholar]
  44. Schulz, H. R., Fabianek, A., Pellicioli, E. C., Hennecke, H. & Thony-Meyer, L. ( 1999; ). Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB. Proc Natl Acad Sci U S A 96, 6462–6467.[CrossRef]
    [Google Scholar]
  45. Schulze, M. & Rodel, G. ( 1989; ). 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 216, 37–43.[CrossRef]
    [Google Scholar]
  46. Simon, R., Priefer, U. & Pühler, A. ( 1983; ). Vector plasmids for in-vivo and in-vitro manipulations of Gram-negative bacteria. In Molecular Genetics of the Bacterial–Plant Interaction: the Rhizobium meliloti–Medicago sativa System, pp. 98–106. Edited by A. Pühler. Berlin: Springer.
  47. Soberon, M., Lopez, O., Morera, C., Girard, M. L., Tabche, M. L. & Miranda, J. ( 1999; ). Enhanced nitrogen fixation in a Rhizobium etli ntrC mutant that overproduces the Bradyrhizobium japonicum symbiotic terminal oxidase cbb 3. Appl Environ Microbiol 65, 2015–2019.
    [Google Scholar]
  48. Somerville, J. E. & Kahn, M. L. ( 1983; ). Cloning of the glutamine synthetase I gene from Rhizobium meliloti. J Bacteriol 156, 168–176.
    [Google Scholar]
  49. Swem, D. L., Swem, L. R., Setterdahl, A. & Bauer, C. E. ( 2005; ). Involvement of SenC in assembly of cytochrome c oxidase in Rhodobacter capsulatus. J Bacteriol 187, 8081–8087.[CrossRef]
    [Google Scholar]
  50. Tabche, M. L., Garcia, E. G., Miranda, J., Escamilla, J. E. & Soberon, M. ( 1998; ). Rhizobium etli cycHJKL gene locus involved in c-type cytochrome biogenesis: sequence analysis and characterization of two cycH mutants. Gene 208, 215–219.[CrossRef]
    [Google Scholar]
  51. Thony-Meyer, L. ( 2002; ). Cytochrome c maturation: a complex pathway for a simple task? Biochem Soc Trans 30, 633–638.
    [Google Scholar]
  52. Thony-Meyer, L. ( 2003; ). A heme chaperone for cytochrome c biosynthesis. Biochemistry 42, 13099–13105.[CrossRef]
    [Google Scholar]
  53. Thony-Meyer, L., Stax, D. & Hennecke, H. ( 1989; ). An unusual gene cluster for the cytochrome bc 1 complex in Bradyrhizobium japonicum and its requirement for effective root nodule symbiosis. Cell 57, 683–697.[CrossRef]
    [Google Scholar]
  54. Vargas, C., McEwan, A. G. & Downie, J. A. ( 1993; ). Detection of c-type cytochromes using enhanced chemiluminescence. Anal Biochem 209, 323–326.[CrossRef]
    [Google Scholar]
  55. Wu, G. M., Delgado, J., Vargas, C., Davies, A. E., Poole, R. K. & Downie, J. A. ( 1996; ). The cytochrome bc 1 complex but not CycM is necessary for symbiotic nitrogen fixation by Rhizobium leguminosarum. Microbiology 142, 3381–3388.[CrossRef]
    [Google Scholar]
  56. Yeoman, K. H., Delgado, M. J., Wexler, M., Downie, J. A. & Johnston, A. W. ( 1997; ). High affinity iron acquisition in Rhizobium leguminosarum requires the cycHJKL operon and the feuPQ gene products, which belong to the family of two-component transcriptional regulators. Microbiology 143, 127–134.[CrossRef]
    [Google Scholar]
  57. Yurgel, S. N. & Kahn, M. L. ( 2005; ). Sinorhizobium meliloti dctA mutants with partial ability to transport dicarboxylic acids. J Bacteriol 187, 1161–1172.[CrossRef]
    [Google Scholar]
  58. Yurgel, S. N., Soberon, M., Sharypova, L. A., Miranda, J., Morera, C. & Simarov, B. V. ( 1998; ). Isolation of Sinorhizobium meliloti Tn5 mutants with altered cytochrome terminal oxidase expression and improved symbiotic performance. FEMS Microbiol Lett 165, 167–173.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/002634-0
Loading
/content/journal/micro/10.1099/mic.0.2006/002634-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error