1887

Abstract

O-antigen is a component of the outer membrane of Gram-negative bacteria and is one of the most variable cell surface constituents, leading to major antigenic variability. The O-antigen forms the basis for bacterial serotyping. In this study, the O-antigen structure of O66 was established, which differs from the known O-antigen structure of O166 only in one linkage (most likely the linkage between the O-units) and -acetylation. The O-antigen gene clusters of O66 and O166 were found to have similar organizations, the only exception being that in O66, the gene is replaced by a non-coding region. The function of the gene in O166 was confirmed by the construction and analysis of deletion and -complementation mutants. It is proposed that a functional gene located outside the O-antigen gene cluster is involved in O66 O-antigen biosynthesis, as has been reported previously in serogroups A, B and D1. The sequence identity for the corresponding genes between the O-antigen gene clusters of O66 and O166 ranges from 64 to 70 %, indicating that they may originate from a common ancestor. It is likely that after the species divergence, O66 got its specific O-antigen form by inactivation of the gene located in the O-antigen gene cluster and acquisition of two new genes (a gene and a prophage gene for -acetyl modification) both residing outside the O-antigen gene cluster.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.037325-0
2010-06-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/6/1642.html?itemId=/content/journal/micro/10.1099/mic.0.037325-0&mimeType=html&fmt=ahah

References

  1. Alexander D. C., Valvano M. A. 1994; Role of the rfe gene in the biosynthesis of the Escherichia coli O7-specific lipopolysaccharide and other O-specific polysaccharides containing N-acetylglucosamine. J Bacteriol 176:7079–7084
    [Google Scholar]
  2. Ali T., Weintraub A., Widmalm G. 2007; Structural determination of the O-antigenic polysaccharide from Escherichia coli O166. Carbohydr Res 342:274–278
    [Google Scholar]
  3. Bastin D. A., Reeves P. R. 1995; Sequence and analysis of the O antigen gene ( rfb) cluster of Escherichia coli O111. Gene 164:17–23
    [Google Scholar]
  4. Bastin D. A., Brown P. K., Haase A., Stevenson G., Reeves P. R. 1993; Repeat unit polysaccharides of bacteria: a model for polymerisation resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Mol Microbiol 7:725–734
    [Google Scholar]
  5. Daniels C., Vindurampulle C., Morona R. 1998; Overexpression and topology of the Shigella flexneri O-antigen polymerase (Rfc/Wzy. Mol Microbiol 28:1211–1222
    [Google Scholar]
  6. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645
    [Google Scholar]
  7. Franco A. V., Liu D., Reeves P. R. 1998; The Wzz (Cld) protein in Escherichia coli: amino acid sequence variation determines O antigen chain length specificity. J Bacteriol 180:2670–2675
    [Google Scholar]
  8. Gemski P. Jr, Sheahan D. G., Washington O., Formal S. B. 1972; Virulence of Shigella flexneri hybrids expressing Escherichia coli somatic antigens. Infect Immun 6:104–111
    [Google Scholar]
  9. Jansson P.-E., Kenne L., Schweda E. 1987; Nuclear magnetic resonance and conformational studies on monoacetylated methyl d-gluco- and d-galacto-pyranosides. J Chem Soc Perkin 1 2:377–383
    [Google Scholar]
  10. Leontein K., Lönngren J. 1993; Determination of the absolute configuration of sugars by gas-liquid chromatography of their acetylated 2-octyl glycosides. Methods Carbohydr Chem 9:87–89
    [Google Scholar]
  11. Lipkind G. M., Shashkov A. S., Knirel Y. A., Vinogradov E. V., Kochetkov N. K. 1988; A computer-assisted structural analysis of regular polysaccharides on the basis of 13C-n.m.r. data. Carbohydr Res 175:59–75
    [Google Scholar]
  12. Liu B., Senchenkova S. N., Feng L., Perepelov A. V., Xu T., Shevelev S. D., Zhu Y., Shashkov A. S., Zou M. other authors 2006; Structural and molecular characterization of Shigella boydii type 16 O antigen. Gene 380:46–53
    [Google Scholar]
  13. Liu B., Knirel Y. A., Feng L., Perepelov A. V., Senchenkova S. N., Wang Q., Reeves P. R., Wang L. 2008; Structure and genetics of Shigella O antigens. FEMS Microbiol Rev 32:627–653
    [Google Scholar]
  14. Reeves P. R. 1992; Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol Lett 79:509–516
    [Google Scholar]
  15. Robbins P. W., Uchida T. 1962; Studies on the chemical basis of the phage conversion of O-antigens in the E-group Salmonella. Biochemistry 1:323–335
    [Google Scholar]
  16. Samuel G., Reeves P. 2003; Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res 338:2503–2519
    [Google Scholar]
  17. Samuel G., Hogbin J. P., Wang L., Reeves P. R. 2004; Relationships of the Escherichia coli O157, O111, and O55 O-antigen gene clusters with those of Salmonella enterica and Citrobacter freundii, which express identical O antigens. J Bacteriol 186:6536–6543
    [Google Scholar]
  18. Sharp P. M. 1991; Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J Mol Evol 33:23–33
    [Google Scholar]
  19. Skurnik M., Venho R., Bengoechea J. A., Moriyon I. 1999; The lipopolysaccharide outer core of Yersinia enterocolitica serotype O: 3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31:1443–1462
    [Google Scholar]
  20. Wang L., Reeves P. R. 1994; Involvement of the galactosyl-1-phosphate transferase encoded by the Salmonella enterica rfbP gene in O antigen subunit processing. J Bacteriol 176:4348–4356
    [Google Scholar]
  21. Wang L., Reeves P. R. 1998; Organization of Escherichia coli O157 O antigen gene cluster and identification of its specific genes. Infect Immun 66:3545–3551
    [Google Scholar]
  22. Wang L., Andrianopoulos K., Liu D., Popoff M. Y., Reeves P. R. 2002; Extensive variation in the O-antigen gene cluster within one Salmonella enterica serogroup reveals an unexpected complex history. J Bacteriol 184:1669–1677
    [Google Scholar]
  23. Wang W., Perepelov A. V., Feng L., Shevelev S. D., Wang Q., Senchenkova S. N., Han W., Li Y., Shashkov A. S. other authors 2007; A group of Escherichia coli and Salmonella enterica O antigens sharing a common backbone structure. Microbiology 153:2159–2167
    [Google Scholar]
  24. Wang Q., Perepelov A. V., Feng L., Knirel Y. A., Li Y., Wang L. 2009; Genetic and structural analyses of Escherichia coli O107 and O117 O-antigens. FEMS Immunol Med Microbiol 55:47–54
    [Google Scholar]
  25. Westphal O., Jann K. 1965; Bacterial lipopolysaccharides. Extraction with phenol–water and further applications of the procedure. In Methods in Carbohydrate Chemistry 5 pp 83–91 Edited by Whistler R. L. New York, London: Academic Press;
    [Google Scholar]
  26. Yu D., Ellis H. M., Lee E. C., Jenkins N. A., Copeland N. G., Court D. L. 2000; An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97:5978–5983
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.037325-0
Loading
/content/journal/micro/10.1099/mic.0.037325-0
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