Skip to content
1887

Microbiology Society logo Microbiology

Volume 153, Issue 7

A group of and O antigens sharing a common backbone structure Free

Abstract

The O-antigen moiety of the LPS is one of the most variable cell surface components of the Gram-negative bacterial outer membrane. Variation is due to the presence of different sugars and sugar linkages. Here, it is reported that a group of O serogroups (O17, O44, O73, O77 and O106), and the serogroup O : 6,14 (H), share a common four-sugar backbone O-subunit structure, and possess almost identical O-antigen gene clusters. Whereas the O77 antigen does not have any substitutions, the other O antigens in this group differ by the addition of one or two glucose side branches at various positions of the backbone. The O-antigen gene clusters for all members of the group encode only the proteins required for biosynthesis of the common four-sugar backbone. The identification of three genes within a putative prophage in the O44 genome is also reported; these genes are presumably involved in the glucosylation of the basic tetrasaccharide unit. This was confirmed by deletion of one of the genes, which encodes a putative glucosyltransferase. Structural analysis of the O antigen produced by the mutant strain demonstrated the absence of glucosylation. An O-antigen structure shared by five and one serogroups, all of which have a long evolutionary history, suggests that the common backbone may be important for the survival of strains in the environment, or for their pathogenicity.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): GlcNAc, N-acetyl-d-glucosamine , ROESY, rotating Overhauser effect spectroscopy and TOCSY, total correlation spectroscopy
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/004192-0
2007-07-01
2025-03-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/7/2159.html?itemId=/content/journal/micro/10.1099/mic.0.2007/004192-0&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. Allison G. E., Verma N. K. 2000; Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol 8:17–23 [CrossRef]
     [Google Scholar]
  3. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
     [Google Scholar]
  4. 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 [CrossRef]
     [Google Scholar]
  5. Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy S. R., Griffiths-Jones S., Howe K. L., Marshall M., Sonnhammer E. L. 2002; The Pfam protein families database. Nucleic Acids Res 30:276–280 [CrossRef]
     [Google Scholar]
  6. Bielaszewska M., Fell M., Greune L., Prager R., Fruth A., Tschape H., Schmidt M. A., Karch H. 2004; Characterization of cytolethal distending toxin genes and expression in shiga toxin-producing Escherichia coli strains of non-O157 serogroups. Infect Immun 72:1812–1816 [CrossRef]
     [Google Scholar]
  7. Campbell A. 2003; Prophage insertion sites. Res Microbiol 154:277–282 [CrossRef]
     [Google Scholar]
  8. Coimbra R. S., Grimont F., Lenormand P., Burguiere P., Beutin L., Grimont P. A. 2000; Identification of Escherichia coli O-serogroups by restriction of the amplified O-antigen gene cluster (rfb-RFLP). Res Microbiol 151:639–654 [CrossRef]
     [Google Scholar]
  9. Comeron J. M. 1999; K -Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15:763–764 [CrossRef]
     [Google Scholar]
  10. Conrad H. E. 1972; Methylation of carbohydrates with methyl iodide in dimethyl sulfoxide in the presence of methylsulfinylanion. Methods Carbohydr Chem 6:361–364
     [Google Scholar]
  11. Daniels C., Vindurampulle C., Morona R. 1998; Overexpression and topology of the Shigella flexneri O-antigen polymerase (Rfc/Wzy). Mol Microbiol 28:1211–1222 [CrossRef]
     [Google Scholar]
  12. 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 [CrossRef]
     [Google Scholar]
  13. di Fabio J. L., Brisson J. R., Perry M. B. 1988; Structure of the major lipopolysaccharide antigenic O-chain produced by Salmonella carrau (O : 6, 14, 24). Carbohydr Res 179:233–244 [CrossRef]
     [Google Scholar]
  14. Fitzgerald C., Sherwood R., Gheesling L. L., Brenner F. W., Fields P. I. 2003; Molecular analysis of the rfb O antigen gene cluster of Salmonella enterica serogroup O : 6,14 and development of a serogroup-specific PCR assay. Appl Environ Microbiol 69:6099–6105 [CrossRef]
     [Google Scholar]
  15. Gerwig G. J., Kamerling J. P., Vliegenthart J. F. G. 1979; Determination of the absolute configuration of monosaccharides in complex carbohydrates by capillary GLC. Carbohydr Res 77:1–7 [CrossRef]
     [Google Scholar]
  16. Hirokawa T., Boon-Chieng S., Mitaku S. 1998; sosui: Classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379 [CrossRef]
     [Google Scholar]
  17. Jansson P. E., Kenne L., Widmalm G. 1989; Computer-assisted structural analysis of polysaccharides with an extended version of CASPER using 1H- and 13C-n.m.r. data. Carbohydr Res 188:169–191 [CrossRef]
     [Google Scholar]
  18. Lee S. J., Romana L. K., Reeves P. R. 1992; Sequence and structural analysis of the rfb (O antigen) gene cluster from a group C1 Salmonella enterica strain. J Gen Microbiol 138:1843–1855 [CrossRef]
     [Google Scholar]
  19. Leontein K., Lindberg B., Lonngren J. 1978; Assignment of absolute configuration of sugars by GLC of their acetylated glycosides formed from chiral alcohols. Carbohydr Res 62:359–362 [CrossRef]
     [Google Scholar]
  20. 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 [CrossRef]
     [Google Scholar]
  21. Liu D., Cole R., Reeves P. R. 1996; An O-antigen processing function for Wzx(RfbX): a promising candidate for O-unit flippase. J Bacteriol 178:2102–2107
     [Google Scholar]
  22. Masoud H., Perry M. B. 1996; Structural characterization of the O-antigenic polysaccharide of Escherichia coli serotype O17 lipopolysaccharide. Biochem Cell Biol 74:241–248 [CrossRef]
     [Google Scholar]
  23. Morona R., Daniels C., Van Den Bosch L. 2003; Genetic modulation of Shigella flexneri 2a lipopolysaccharide O antigen modal chain length reveals that it has been optimized for virulence. Microbiology 149:925–939 [CrossRef]
     [Google Scholar]
  24. Nataro J. P., Kaper J. B. 1998; Diarrheagenic Escherichia coli. Clin Microbiol Rev 11:142–201
     [Google Scholar]
  25. Ochman H., Wilson A. C. 1987a; Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86 [CrossRef]
     [Google Scholar]
  26. Ochman H., Wilson A. C. others 1987b; Evolutionary history of enteric bacteria. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp 1649–1654 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  27. Reeves P. P., Wang L. 2002; Genomic organization of LPS-specific loci. Curr Top Microbiol Immunol 264:109–135
     [Google Scholar]
  28. 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 [CrossRef]
     [Google Scholar]
  29. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M. A., Barrell B. 2000; Artemis: sequence visualisation and annotation. Bioinformatics 16:944–945 [CrossRef]
     [Google Scholar]
  30. 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 [CrossRef]
     [Google Scholar]
  31. Shepherd J. G., Wang L., Reeves P. R. 2000; Comparison of O-antigen gene clusters of Escherichia coli ( Shigella ) sonnei and Plesiomonas shigelloides O17: sonnei gained its current plasmid-borne O-antigen genes from P. shigelloides in a recent event. Infect Immun 68:6056–6061 [CrossRef]
     [Google Scholar]
  32. Staaf M., Widmalm G., Weintraub A., Nataro J. P. 1995; Structural elucidation of the O-antigenic polysaccharide from Escherichia coli O44 : H18. Eur J Biochem 233:473–477 [CrossRef]
     [Google Scholar]
  33. Staden R. 1996; The Staden sequence analysis package. Mol Biotechnol 5:233–241 [CrossRef]
     [Google Scholar]
  34. Tarr P. I., Schoening L. M., Yea Y. L., Ward T. R., Jelacic S., Whittam T. S. 2000; Acquisition of the rfb-gnd cluster in evolution of Escherichia coli O55 and O157. J Bacteriol 182:6183–6191 [CrossRef]
     [Google Scholar]
  35. Tatusov R. L., Natale D. A., Garkavtsev I. V., Tatusova T. A., Shankavaram U. T., Rao B. S., Kiryutin B., Galperin M. Y., Fedorova N. D., Koonin E. V. 2001; The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28 [CrossRef]
     [Google Scholar]
  36. Van den Bosch L., Morona R. 2003; The actin-based motility defect of a Shigella flexneri rmlD rough LPS mutant is not due to loss of IcsA polarity. Microb Pathog 35:11–18 [CrossRef]
     [Google Scholar]
  37. 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]
  38. 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]
  39. Wang L., Reeves P. R. 2000; The Escherichia coli O111 and Salmonella enterica O35 gene clusters: gene clusters encoding the same colitose-containing O antigen are highly conserved. J Bacteriol 182:5256–5261 [CrossRef]
     [Google Scholar]
  40. Wang L., Briggs C. E., Rothemund D., Fratamico P., Luchansky J. B., Reeves P. R. 2001a; Sequence of the E. coli O104 antigen gene cluster and identification of O104-specific genes. Gene 270:231–236 [CrossRef]
     [Google Scholar]
  41. Wang L., Qu W., Reeves P. R. 2001b; Sequence analysis of four Shigella boydii O-antigen loci: implication for Escherichia coli and Shigella relationships. Infect Immun 69:6923–6930 [CrossRef]
     [Google Scholar]
  42. West N. P., Sansonetti P., Mounier J., Exley R. M., Parsot C., Guadagnini S., Prevost M. C., Prochnicka-Chalufour A., Delepierre M. other authors 2005; Optimization of virulence functions through glucosylation of Shigella LPS. Science 307:1313–1317 [CrossRef]
     [Google Scholar]
  43. Yildirim H., Weintraub A., Widmalm G. 2001; Structural studies of the O-polysaccharide from the Escherichia coli O77 lipopolysaccharide. Carbohydr Res 333:179–183 [CrossRef]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.2007/004192-0
Loading
A group of Escherichia coli and Salmonella enterica O antigens sharing a common backbone structure
Microbiology 153, 2159 (2007); https://doi.org/10.1099/mic.0.2007/004192-0
/content/journal/micro/10.1099/mic.0.2007/004192-0
/content/journal/micro/10.1099/mic.0.2007/004192-0
Loading

Data & Media loading...

Most cited 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