1887

Microbiology

Volume 150, Issue 2

CtaG is required for formation of active cytochrome oxidase in Free

Abstract

The Gram-positive bacterium contains two respiratory oxidases of the haem-copper superfamily: cytochrome , which is a quinol oxidase, and cytochrome , which is a cytochrome oxidase. Cytochrome oxidase uniquely contains a di-copper centre, Cu. CtaG is a membrane protein encoded by the same gene cluster as that which encodes the subunits of cytochrome oxidase. The role of CtaG and orthologous proteins present in many other Gram-positive bacteria has remained unexplored. The sequence of CtaG is unrelated to that of CtaG/Cox11p of proteobacteria and eukaryotic cells. This study shows that CtaG is essential for the formation of active cytochrome but is not required for assembly of the core subunits I and II with haem in the membrane and it has no role in the synthesis of active cytochrome . YpmQ, a homologue to Sco1p of eukaryotic cells, is also a membrane-bound cytochrome oxidase-specific assembly factor. Properties of CtaG- and YpmQ-deficient mutants were compared. Cells lacking YpmQ showed a low cytochrome oxidase activity and this defect was suppressed by the supplementation of the growth medium with copper ions. It has previously been proposed that YpmQ/Sco1p is involved in synthesis of the Cu centre. The results of this study are consistent with this proposal but the exact role of YpmQ in assembly of cytochrome oxidase remains to be elucidated.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): ICP-MS, inductively coupled plasma emission mass spectroscopy and TMPD, N,N,N′N′-tetramethyl-p-phenylenediamine
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26691-0
2004-02-01
2021-04-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/2/mic1500415.html?itemId=/content/journal/micro/10.1099/mic.0.26691-0&mimeType=html&fmt=ahah

References

  1. Barrientos A., Barros M. H., Valnot I., Tzagoloff A, Rötig A., Rustin P. 2002; Cytochrome oxidase in health and disease. Gene 286:53–63 [CrossRef]
     [Google Scholar]
  2. Beers J., Glerum D. M., Tzagoloff A. 2002; Purification and characterization of yeast Sco1p, a mitochondrial copper protein. J Biol Chem 277:22185–22190 [CrossRef]
     [Google Scholar]
  3. Bengtsson J. 2001 Genes for cytochrome c and cytochrome c oxidase synthesis in Bacillus subtilis PhD thesis Lund University;
     [Google Scholar]
  4. Bengtsson J., Tjalsma H., Rivolta C., Hederstedt L. 1999; Subunit II of Bacillus subtilis cytochrome c oxidase is a lipoprotein. J Bacteriol 181:685–688
     [Google Scholar]
  5. Bratton M. R., Hiser L., Antholine W. E., Hoganson C., Hosler J. P. 2000; Identification of the structural subunits required for formation of the metal centers in subunit I of cytochrome c oxidase of Rhodobacter sphaeroides . Biochemistry 39:12989–12995 [CrossRef]
     [Google Scholar]
  6. Carr H. S., George G. N., Winge D. R. 2002; Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I)-binding protein. J Biol Chem 277:31237–31242 [CrossRef]
     [Google Scholar]
  7. Chinenov Y. V. 2000; Cytochrome c oxidase assembly factors with a thioredoxin fold are conserved among prokaryotes and eukaryotes. J Mol Med 78:239–242 [CrossRef]
     [Google Scholar]
  8. Dickinson E. K., Adams D. L., Schon E. A., Glerum D. M. 2000; A human SCO2 mutation helps define the role of Sco1p in the cytochrome oxidase assembly pathway. J Biol Chem 275:26780–26785
     [Google Scholar]
  9. Fortnagel P., Freese E. 1968; Analysis of sporulation mutants: II. Mutants blocked in the citric acid cycle. J Bacteriol 95:1431–1438
     [Google Scholar]
  10. Guérout-Fleury A.-M., Shazand K., Frandsen N., Stragier P. 1995; Antibiotic-resistance cassettes for Bacillus subtilis . Gene 167:335–336 [CrossRef]
     [Google Scholar]
  11. Hederstedt L. 1986; Molecular properties, genetics, and biosynthesis of Bacillus subtilis succinate dehydrogenase complex. Methods Enzymol 126:399–414
     [Google Scholar]
  12. Hiser L., Di Valentin M., Hamer A. G., Hosler J. P. 2000; Cox11p is required for stable formation of the CuB and magnesium centers of cytochrome c oxidase. J Biol Chem 275:619–623 [CrossRef]
     [Google Scholar]
  13. Hoch J. A. 1991; Genetic analysis in Bacillus subtilis . Methods Enzymol 204:305–320
     [Google Scholar]
  14. Ish-Horowicz D., Burke J. F. 1981; Rapid and efficient cosmid cloning. Nucleic Acids Res 9:2989–2998 [CrossRef]
     [Google Scholar]
  15. Johansson P., Hederstedt L. 1999; Organization of genes for tetrapyrrole biosynthesis in Gram-positive bacteria. Microbiology 145:529–538 [CrossRef]
     [Google Scholar]
  16. Kunst F., Ogasawara N., Moszer I. 148 other authors 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis . Nature 390:249–256 [CrossRef]
     [Google Scholar]
  17. 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]
  18. Lemma E., Schägger H., Kröger A. 1993; The menaquinol oxidase of Bacillus subtilis W23. Arch Microbiol 159:574–578 [CrossRef]
     [Google Scholar]
  19. Liu X., Taber H. W. 1998; Catabolite regulation of the Bacillus subtilis ctaBCDEF gene cluster. J Bacteriol 180:6154–6163
     [Google Scholar]
  20. Lode A., Kuschel M., Paret C., Rödel G. 2000; Mitochondrial copper metabolism in yeast: interaction between Sco1p and Cox2p. FEBS Lett 485:19–24 [CrossRef]
     [Google Scholar]
  21. Marmur J. 1961; A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218 [CrossRef]
     [Google Scholar]
  22. Mattatall N. R., Jazairi J., Hill B. C. 2000; Characterization of YmpQ, an accessory protein required for the expression of cytochrome c oxidase in Bacillus subtilis . J Biol Chem 275:28802–28809 [CrossRef]
     [Google Scholar]
  23. McEwan A. G., Lewin A., Davy S. L., Boetzel R., Leech A., Walker D., Wood T., Moore G. R. 2002; PrrC from Rhodobacter sphaeroides , a homologue of eukaryotic Sco proteins, is a copper-binding protein and may have a thiol-disulfide oxidoreductase activity. FEBS Lett 518:10–16 [CrossRef]
     [Google Scholar]
  24. Michel H., Behr J., Harrenga A., Kannt A. 1998; Cytochrome oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27:329–356 [CrossRef]
     [Google Scholar]
  25. Nittis T., George G. N., Winge D. R. 2001; Yeast Sco1, a protein essential for cytochrome c oxidase function, is a Cu(I)-binding protein. J Biol Chem 276:42520–42526 [CrossRef]
     [Google Scholar]
  26. Powers L., Lauraeus M., Reddy K. S., Chance B., Wikström M. 1994 Structure of the binuclear heme iron-copper site in the quinol-oxidizing cytochrome aa 3 from Bacillus subtilis Biochim Biophys Acta; 1183504–512 [CrossRef]
     [Google Scholar]
  27. Punter F. A., Glerum D. M. 2003; Mutagenesis reveals a specific role for Cox17p in copper transport to cytochrome oxidase. J Biol Chem 278:30875–30880 [CrossRef]
     [Google Scholar]
  28. Rentzsch A., Krummeck-Weiss G., Hofer A., Bartuschka A., Ostermann K., Rödel G. 1999; Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr Genet 35:103–108 [CrossRef]
     [Google Scholar]
  29. Salviati L., Hernandez-Rosa E., Walker W. F., Sacconi S., DiMauro S., Schon E. A., Davidson M. M. 2002; Copper supplementation restores cytochrome c oxidase activity in cultured cells from patients with SCO2 mutations. Biochem J 363:321–327 [CrossRef]
     [Google Scholar]
  30. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  31. Santana M., Kunst F., Hullo M. F., Rapoport G., Danchin A., Glaser P. 1992; Molecular cloning, sequencing and physiological characterisation of the qox operon from Bacillus subtilis encoding the aa 3-600 quinol oxidase. J Biol Chem 267:10225–10231
     [Google Scholar]
  32. Saraste M., Metso T., Nakari T., Jalli T., Lauraaeus M., van der Oost J. 1991; The Bacillus subtilis cytochrome- c oxidase. Variations on a conserved theme. Eur J Biochem 195:517–525 [CrossRef]
     [Google Scholar]
  33. Schägger H., von Jagow G. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [CrossRef]
     [Google Scholar]
  34. Schiött T., von Wachenfeldt C., Hederstedt L. 1997a; Identification and characterization of the ccdA gene required for cytochrome c synthesis in Bacillus subtilis . J Bacteriol 179:1962–1973
     [Google Scholar]
  35. Schiött T., Trone-Holst M., Hederstedt L. 1997b; Bacillus subtilis CcdA defective mutants are blocked in a late step of cytochrome c biogenesis. J Bacteriol 179:4523–4529
     [Google Scholar]
  36. Schumann W., Ehrlich S. D., Ogasawara N. 2001 Functional Analysis of Bacterial Genes New York: Wiley;
     [Google Scholar]
  37. Seib K. L., Jennings M. P., McEwan A. G. 2003; A Sco homologue plays a role in defence against oxidative stress in pathogenic Neisseria . FEBS Lett 546:411–415 [CrossRef]
     [Google Scholar]
  38. Stragier P., Bonamy C., Karmazyn-Campelli C. 1988; Processing of a sporulation sigma factor in Bacillus subtilis . How morphological structure could control gene expression. Cell 532:697–704
     [Google Scholar]
  39. Svensson B., Lübben M., Hederstedt L. 1993; Bacillus subtilis CtaA and CtaB function in haem A biosynthesis. Mol Microbiol 10:193–201 [CrossRef]
     [Google Scholar]
  40. Tatusov R. L., Natale D. A., Garkavtsev I. V. 7 other authors 2001; The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28 [CrossRef]
     [Google Scholar]
  41. Thöny-Meyer L. 1997; Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61:337–376
     [Google Scholar]
  42. Tzagoloff A., Dieckman C. C. 1990; PET genes of Saccharomyces cerevisiae . Microbiol Rev 54:211–225
     [Google Scholar]
  43. van der Oost J., von Wachenfeldt C., Hederstedt L., Saraste M. 1991; Bacillus subtilis cytochrome oxidase mutants: biochemical analysis and genetic evidence for two aa 3-type oxidases. Mol Microbiol 5:2063–2072 [CrossRef]
     [Google Scholar]
  44. von Wachenfeldt C., Hederstedt L. 1992; Molecular biology of Bacillus subtilis cytochromes. FEMS Microbiol Lett 100:91–100 [CrossRef]
     [Google Scholar]
  45. von Wachenfeldt C., Hederstedt L. 1993; Physico-chemical characterisation of membrane-bound and water-soluble forms of Bacillus subtilis cytochrome c -550. Eur J Biochem 212:499–509 [CrossRef]
     [Google Scholar]
  46. von Wachenfeldt C., Hederstedt L. 2002; Respiratory cytochromes, other heme proteins, and heme biosynthesis. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp 163–179 Edited by Sonenshein A. L., Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  47. von Wachenfeldt C., de Vries S., van der Oost J. 1994; The CuA site of the caa 3-type oxidase of Bacillus subtilis is a mixed-valence binuclear copper center. FEBS Lett 340:109–113 [CrossRef]
     [Google Scholar]
  48. Winstedt L., von Wachenfeldt C. 2000; Terminal oxidases of Bacillus subtilis strain 168: one quinol oxidase, cytochrome aa 3 or cytochrome bd , is required for aerobic growth. J Bacteriol 182:6557–6564 [CrossRef]
     [Google Scholar]
  49. Winstedt L., Youshida K., Fujita Y., von Wachenfeldt C. 1998; Cytochrome bd biosynthesis in Bacillus subtilis : characterization of the cydABCD operon. J Bacteriol 180:6571–6580
     [Google Scholar]
  50. Yu J., Hederstedt L., Piggot P. 1995; The cytochrome bc complex (menaquinol : cytochrome c reductase) in Bacillus subtilis has a non-traditional subunit organization. J Bacteriol 177:6751–6760
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26691-0
Loading
CtaG is required for formation of active cytochrome c oxidase in Bacillus subtilis
Microbiology 150, 415 (2004); https://doi.org/10.1099/mic.0.26691-0
/content/journal/micro/10.1099/mic.0.26691-0
/content/journal/micro/10.1099/mic.0.26691-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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