1887

Abstract

Three -type cytochromes were identified in , based on predictions from genome sequences, that were hypothesized to be involved in electron transport to terminal electron acceptor reductases for oxygen (the cytochrome oxidase) and nitrite (the nitrite reductase, AniA). Mutants were generated by allelic exchange with disrupted copies of the genes encoding these cytochromes and the phenotypes of the resultant mutants analysed. It was found that cytochrome is required for nitrite reductase activity, whereas cytochromes and are both required for efficient growth using oxygen as an electron acceptor. Mutants in , , and + have a decreased capacity to reduce oxygen, but there is a background oxygen-reduction activity, indicating that there may be other routes for electron transfer from the cytochrome complex to the cytochrome oxidase, whereas cytochrome appears to be the sole route of electrons to the nitrite reductase in . Interestingly, cytochrome is highly similar to a domain of copper nitrite reductases from various proteobacteria, whereas cytochrome has high identity with a domain of the cytochrome oxidase of , yet these two proteins function in oxygen respiration and nitrite respiration, respectively. This highlights a limitation of predicting protein function from similarity to known proteins, i.e. very closely related protein domains in different organisms can have different redox partners.

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2008-09-01
2024-04-24
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References

  1. Anjum M. F., Stevanin T. M., Read R. C., Moir J. W. B. 2002; Nitric oxide metabolism in Neisseria meningitidis . J Bacteriol 184:2987–2993
    [Google Scholar]
  2. Bartalesi I., Bertini I., Hajieva P., Rosato A., Vasos P. R. 2002; Solution structure of a monoheme ferrocytochrome c from Shewanella putrefaciens and structural analysis of sequence-similar proteins: functional implications. Biochemistry 41:5112–5119
    [Google Scholar]
  3. Bogdan J. A., Minetti C. A., Blake M. S. 2002; A one step method for genetic transformation of non-piliated Neisseria meningitidis . J Microbiol Methods 49:97–101
    [Google Scholar]
  4. Boulanger M. J., Murphy M. E. 2002; Crystal structure of the soluble domain of the major anaerobically induced outer membrane protein (AniA) from pathogenic Neisseria : a new class of copper-containing nitrite reductases. J Mol Biol 315:1111–1127
    [Google Scholar]
  5. Brook I. 2003; Microbial dynamics of purulent nasopharyngitis in children. Int J Pediatr Otorhinolaryngol 67:1047–1053
    [Google Scholar]
  6. Clark V. L., Campbell L. A., Palermo D. A., Evans T. M., Klimpel K. W. 1987; Induction and repression of outer membrane proteins by anaerobic growth of Neisseria gonorrhoeae . Infect Immun 55:1359–1364
    [Google Scholar]
  7. Deeudom M., Rock J., Moir J. W. B. 2006; Organization of the respiratory chain of Neisseria meningitidis . Biochem Soc Trans 34:139–142
    [Google Scholar]
  8. de Vries S., Schröder I. 2002; Comparison between the nitric oxide reductase family and its aerobic relatives, the cytochrome oxidases. Biochem Soc Trans 30:662–667
    [Google Scholar]
  9. Diederix R. E. M., Ubbink M., Canters G. W. 2002; Peroxidase activity as a tool for studying the folding of c -type cytochromes. Biochemistry 41:13067–13077
    [Google Scholar]
  10. Gotschlich E. C., Seiff M. E. 1987; Identification and gene structure of an azurin-like protein with a lipoprotein signal peptide in Neisseria gonorrhoeae . FEMS Microbiol Lett 43:253–255
    [Google Scholar]
  11. Hoehn G. T., Clark V. L. 1992; The major anaerobically induced outer membrane protein of Neisseria gonorrhoeae , Pan1, is a lipoprotein. Infect Immun 60:4704–4708
    [Google Scholar]
  12. Kadziola A., Larsen S. 1997; Crystal structure of the di-haem cytochrome c 4 from Pseudomonas stutzeri determined at 2.2 Å resolution. Structure 5:203–216
    [Google Scholar]
  13. Kawula T. H., Spinol S. M., Klapper D. G., Cannon J. G. 1987; Localization of a conserved epitope and an azurin-like domain in the H.8 protein of pathogenic Neisseria . Mol Microbiol 1:179–185
    [Google Scholar]
  14. Matias V. R., Al-Amoudi A., Dubochet J., Beveridge T. J. 2003; Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa . J Bacteriol 185:6112–6118
    [Google Scholar]
  15. McGuinness B. T., Clarke I. N., Lambden P. R., Barlow A. K., Poolman J. T., Jones D. M., Heckels J. E. 1991; Point mutation in meningococcal porA gene associated with increased endemic disease. Lancet 337:514–517
    [Google Scholar]
  16. Moir J. W. B., Baratta D., Richardson D. J., Ferguson S. J. 1993; The purification of a cd 1-type nitrite reductase and the absence of a copper-type nitrite reductase from the aerobic denitrifier Thiosphaera pantotropha ; the role of pseudoazurin as an electron donor. Eur J Biochem 212:377–385
    [Google Scholar]
  17. Muresanu L., Pristovsek P., Löhr F., Maneg O., Mukrasch M. D., Rüterjans H., Ludwig B., Lücke C. 2006; The electron transfer complex between cytochrome c 552 and the CuA domain of the Thermus thermophilus ba 3 oxidase. A combined NMR and computational approach. J Biol Chem 281:14503–14513
    [Google Scholar]
  18. Pitcher R. S., Watmough N. J. 2004; The bacterial cytochrome cbb 3 oxidases. Biochim Biophys Acta 1655:388–399
    [Google Scholar]
  19. Prentki P., Krisch H. M. 1984; In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313
    [Google Scholar]
  20. Rock J. D., Mahnane M. R., Anjum M. F., Shaw J. G., Read R. C., Moir J. W. B. 2005; The pathogen Neisseria meningitidis requires oxygen, but supplements growth by denitrification. Nitrite, nitric oxide and oxygen control respiratory flux at genetic and metabolic levels. Mol Microbiol 58:800–809
    [Google Scholar]
  21. Rock J. D., Thomson M. J., Read R. C., Moir J. W. B. 2007; Regulation of denitrification genes in Neisseria meningitidis by nitric oxide and the repressor NsrR. J Bacteriol 189:1138–1144
    [Google Scholar]
  22. Tamura N., Murakami S., Oyama Y., Ishiguro M., Yamaguchi A. 2005; Direct interaction of multidrug efflux transporter AcrB and outer membrane channel TolC detected via site-directed disulfide cross-linking. Biochemistry 44:11115–11121
    [Google Scholar]
  23. Turner S. M., Moir J. W. B., Griffiths L., Smith H., Cole J. A. 2005; Genomic analysis of the c -type cytochromes of Neisseria gonorrhoeae : mutational and biochemical analysis of cytochrome c ′, a nitric oxide-binding lipoprotein important for adaptation to microaerobic growth and its implications for pathogenicity. Biochem J 388:545–553
    [Google Scholar]
  24. van Deuren M., Brandtzaeg P., van der Meer J. W. M. 2000; Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13:144–166
    [Google Scholar]
  25. Vargas C., McEwan A. G., Downie J. A. 1993; Detection of c -type cytochromes using enhanced chemiluminescence. Anal Biochem 209:323–326
    [Google Scholar]
  26. Wu H. J., Seib K. L., Edwards J. L., Apicella M. A., McEwan A. G., Jennings M. P. 2005; Azurin of pathogenic Neisseria spp. is involved in defense against hydrogen peroxide and survival within cervical epithelial cells. Infect Immun 73:8444–8448
    [Google Scholar]
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