1887

Abstract

The genome of serogroup B strain MC58 contains three genes – , and – encoding putative homologues of DsbA, a periplasmic thiol disulphide oxidoreductase protein-folding catalyst of the Dsb protein family. DsbA assists the folding of periplasmic and membrane proteins in diverse organisms. While all three cloned genes complemented the DTT sensitivity of -null , they showed different activities in folding specific target proteins in this background. NMB0278 protein was the most active in complementing defects in motility and alkaline phosphatase activity, while NMB0294 was the most active in folding periplasmic MalF. NMB0407 showed the weakest activity in all assays. It is extremely unusual for organisms to contain more than one chromosomal . Among the members of the genus , only the meningococcus carries all three of these genes. Strains of , , and contained only homologues of and , while , and carried only . It is speculated that the versatility of the meningococcus in surviving in different colonizing and invasive disease settings may be derived in part from an enhanced potential to deploy outer-membrane proteins, a consequence of carrying an extended repertoire of protein-folding catalysts.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27216-0
2004-09-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/9/mic1502993.html?itemId=/content/journal/micro/10.1099/mic.0.27216-0&mimeType=html&fmt=ahah

References

  1. Bader M., Muse W., Ballou D. P., Gassner C., Bardwell J. C. 1999; Oxidative protein folding is driven by the electron transport system. Cell 98:217–227 [CrossRef]
    [Google Scholar]
  2. Bardwell J. C., McGovern K., Beckwith J. 1991; Identification of a protein required for disulphide bond formation in vivo. Cell 67:581–589 [CrossRef]
    [Google Scholar]
  3. Bouwman C. W., Kohli M., Killoran A., Touchie G. A., Kadner R. J., Martin N. L. 2003; Characterization of SrgA, a Salmonella enterica serovar Typhimurium virulence plasmid-encoded paralogue of the disulfide oxidoreductase DsbA, essential for biogenesis of plasmid-encoded fimbriae. J Bacteriol 185:991–1000 [CrossRef]
    [Google Scholar]
  4. Brickman E., Beckwith J. 1975; Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and π80 transducing phages. J Mol Biol 96:307–316 [CrossRef]
    [Google Scholar]
  5. Chung J., Chen T., Missiakas D. 2000; Transfer of electrons across the cytoplasmic membrane by DsbD, a membrane protein involved in thiol-disulphide exchange and protein folding in the bacterial periplasm. Mol Microbiol 35:1099–1109 [CrossRef]
    [Google Scholar]
  6. Dailey F. E., Berg H. C. 1993; Mutants in disulphide bond formation that disrupt flagellar assembly in Escherichia coli. Proc Natl Acad Sci U S A 90:1043–1047 [CrossRef]
    [Google Scholar]
  7. Fabianek R. A., Hennecke H., Thony-Meyer L. 1998; The active-site cysteines of the periplasmic thioredoxin-like protein CcmG of Escherichia coli are important but not essential for cytochrome c maturation in vivo. J Bacteriol 180:1947–1950
    [Google Scholar]
  8. Gonnet G. H. 1994; New algorithms for the computation of evolutionary phylogenetic trees. In Computational Methods in Genome Research pp. 153–161 Edited by Suhai S. New York: Plenum;
    [Google Scholar]
  9. Gonnet G. H., Cohen M. A., Benner S. A. 1992; Exhaustive matching of the entire protein sequence database. Science 256:1443–1445 [CrossRef]
    [Google Scholar]
  10. Gonnet G. H., Hallett M. T., Korostensky C., Bernardin L. 2000; Darwin v. 2.0: an interpreted computer language for the biosciences. Bioinformatics 16:101–103 [CrossRef]
    [Google Scholar]
  11. Grauschopf U., Winther J. R., Korber P., Zander T., Dallinger P., Bardwell J. C. 1995; Why is DsbA such an oxidizing disulfide catalyst?. Cell 83:947–955 [CrossRef]
    [Google Scholar]
  12. Guilhot C., Jander G., Martin N. L., Beckwith J. 1995; Evidence that the pathway of disulphide bond formation in Escherichia coli involves interactions between the cysteines of DsbA and DsbB. Proc Natl Acad Sci U S A 92:9895–9899 [CrossRef]
    [Google Scholar]
  13. Kim E. E., Wyckoff H. W. 1991; Reaction mechanism of alkaline phosphatase based on crystal structures. Two-metal ion catalysis. J Mol Biol 218:449–464 [CrossRef]
    [Google Scholar]
  14. Klee S. R., Nassif X., Kusecek B., Merker P., Beretti J. L., Achtman M., Tinsley C. R. 2000; Molecular and biological analysis of eight genetic islands that distinguish Neisseria meningitidis from the closely related pathogen Neisseria gonorrhoeae. Infect Immun 68:2082–2095 [CrossRef]
    [Google Scholar]
  15. Martin J. L., Bardwell J. C., Kuriyan J. 1993; Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365:464–468 [CrossRef]
    [Google Scholar]
  16. Mathews F. S. 1985; The structure, function and evolution of cytochromes. Prog Biophys Mol Biol 45:1–56 [CrossRef]
    [Google Scholar]
  17. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  18. Missiakas D., Raina S. 1997; Protein folding in the bacterial periplasm. J Bacteriol 179:2465–2471
    [Google Scholar]
  19. Perrin A., Bonacorsi S., Carbonnelle E., Talibi D., Dessen P., Nassif X., Tinsley C. 2002; Comparative genomics identifies the genetic islands that distinguish Neisseria meningitidis, the agent of cerebrospinal meningitis, from other Neisseria species. Infect Immun 70:7063–7072 [CrossRef]
    [Google Scholar]
  20. Pizza M., Scarlato V., Masignani V. 33 other authors 2000; Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 287:1816–1820 [CrossRef]
    [Google Scholar]
  21. Sambrook J., Fritch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  22. Sardesai A. A., Genevaux P., Schwager F., Ang D., Georgopoulos C. 2003; The OmpL porin does not modulate redox potential in the periplasmic space of Escherichia coli. EMBO J 22:1461–1466 [CrossRef]
    [Google Scholar]
  23. Tinsley C. R., Voulhoux R., Beretti J. L., Tommassen J., Nassif X. 2004; Three homologues, including two membrane-bound proteins, of the disulfide oxidoreductase DsbA in Neisseria meningitidis: effects on bacterial growth and biogenesis of functional type IV pili. J Biol Chem 279:27078–27087 [CrossRef]
    [Google Scholar]
  24. Turcot I., Ponnampalam T. V., Bouwman C. W., Martin N. L. 2001; Isolation and characterization of a chromosomally encoded disulphide oxidoreductase from Salmonella enterica serovar Typhimurium. Can J Microbiol 47:711–721 [CrossRef]
    [Google Scholar]
  25. Willis R. C., Morris R. G., Cirakoglu C., Schellenberg G. D., Gerber N. H., Furlong C. E. 1974; Preparations of periplasmic proteins from Salmonella typhimurium and Escherichia coli. Arch Biochem Biophys 30:64–75
    [Google Scholar]
  26. Yu J., Kroll J. S. 1999; DsbA: a protein-folding catalyst contributing to bacterial virulence. Microbes Infect 1:1221–1228 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27216-0
Loading
/content/journal/micro/10.1099/mic.0.27216-0
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