1887

Abstract

Mastitis represents one of the most significant health problems of dairy herds. The two major causative agents of this disease are and . Of the first, its lipopolysaccharide (LPS) is thought to play a prominent role during infection. Here, we report the O-antigen (OPS, O-specific polysaccharide) structure of the LPS from bovine mastitis isolate 1303. The structure was determined utilizing chemical analyses, mass spectrometry, and 1D and 2D NMR spectroscopy methods. The O-repeating unit was characterized as -[→4)-β--Qui3NAc-(1→3)-α--Fuc2OAc-(1→4)-β--Gal-(1→3)-α--GalNAc-(1→]- in which the -acetyl substitution was non-stoichiometric. The nucleotide sequence of the O-antigen gene cluster of 1303 was also determined. This cluster, located between the and genes, contains 13 putative open reading frames, most of which represent unknown nucleotide sequences that have not been described before. The O-antigen of 1303 was shown to substitute O-7 of the terminal -heptose of the K-12 core oligosaccharide. Interestingly, the non-OPS-substituted core oligosaccharide represented a truncated version of the K-12 outer core – namely terminal -heptose and glucose were missing; however, it possessed a third Kdo residue in the inner core. On the basis of structural and genetic data we show that the mastitis isolate 1303 represents a new serotype and possesses the K-12 core type, which is rather uncommon among human and bovine isolates.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.046912-0
2011-06-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/6/1750.html?itemId=/content/journal/micro/10.1099/mic.0.046912-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schäffer 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].[PubMed].
    [Google Scholar]
  2. Amor K., Heinrichs D. E., Frirdich E., Ziebell K., Johnson R. P., Whitfield C.. ( 2000;). Distribution of core oligosaccharide types in lipopolysaccharides from Escherichia coli. . Infect Immun 68:, 1116–1124. [CrossRef].[PubMed].
    [Google Scholar]
  3. Andrianopoulos K., Wang L., Reeves P. R. J.. ( 1998;). Identification of the fucose synthetase gene in the colanic acid gene cluster of Escherichia coli K-12. . J Bacteriol 180:, 998–1001.[PubMed].
    [Google Scholar]
  4. 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].[PubMed].
    [Google Scholar]
  5. Brade L., Grimmecke H. D., Holst O., Brabetz W., Zamojski A., Brade H.. ( 1996;). Specificity of monoclonal antibodies against Escherichia coli K-12 lipopolysaccharide. . J Endotoxin Res 3:, 39–47.
    [Google Scholar]
  6. Burvenich C., Van Merris V., Mehrzad J., Diez-Fraile A., Duchateau L.. ( 2003;). Severity of E. coli mastitis is mainly determined by cow factors. . Vet Res 34:, 521–564. [CrossRef].[PubMed].
    [Google Scholar]
  7. Ciucanu I., Kerek F.. ( 1984;). A simple and rapid method for the permethylation of carbohydrates. . Carbohydr Res 131:, 209–217. [CrossRef]
    [Google Scholar]
  8. D’Souza J. M., Wang L., Reeves P.. ( 2002;). Sequence of the Escherichia coli O26 O antigen gene cluster and identification of O26 specific genes. . Gene 297:, 123–127. [CrossRef].[PubMed].
    [Google Scholar]
  9. 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].[PubMed].
    [Google Scholar]
  10. Di Padova F. E., Brade H., Barclay G. R., Poxton I. R., Liehl E., Schuetze E., Kocher H. P., Ramsay G., Schreier M. H. et al. ( 1993;). A broadly cross-protective monoclonal antibody binding to Escherichia coli and Salmonella lipopolysaccharides. . Infect Immun 61:, 3863–3872.[PubMed].
    [Google Scholar]
  11. Feldman M. F., Marolda C. L., Monteiro M. A., Perry M. B., Parodi A. J., Valvano M. A.. ( 1999;). The activity of a putative polyisoprenol-linked sugar translocase (Wzx) involved in Escherichia coli O antigen assembly is independent of the chemical structure of the O repeat. . J Biol Chem 274:, 35129–35138. [CrossRef].[PubMed].
    [Google Scholar]
  12. Frirdich E., Lindner B., Holst O., Whitfield C.. ( 2003;). Overexpression of the waaZ gene leads to modification of the structure of the inner core region of Escherichia coli lipopolysaccharide, truncation of the outer core, and reduction of the amount of O polysaccharide on the cell surface. . J Bacteriol 185:, 1659–1671. [CrossRef].[PubMed].
    [Google Scholar]
  13. Gerwig G. J., Kamerling J. P., Vliegenthart J. F.. ( 1979;). Determination of the absolute configuration of mono-saccharides in complex carbohydrates by capillary G.L.C. . Carbohydr Res 77:, 10–17. [CrossRef].[PubMed].
    [Google Scholar]
  14. Gibbs R. J., Stewart J., Poxton I. R.. ( 2004;). The distribution of, and antibody response to, the core lipopolysaccharide region of Escherichia coli isolated from the faeces of healthy humans and cattle. . J Med Microbiol 53:, 959–964. [CrossRef].[PubMed].
    [Google Scholar]
  15. Ginsburg V.. ( 1961;). Studies on the biosynthesis of guanosine diphosphate l-fucose. . J Biol Chem 236:, 2389–2393.[PubMed].
    [Google Scholar]
  16. Graninger M., Kneidinger B., Bruno K., Scheberl A., Messner P.. ( 2002;). Homologs of the Rml enzymes from Salmonella enterica are responsible for dTDP-β-l-rhamnose biosynthesis in the gram-positive thermophile Aneurinibacillus thermoaerophilus DSM 10155. . Appl Environ Microbiol 68:, 3708–3715. [CrossRef].[PubMed].
    [Google Scholar]
  17. Gray C. H., Tatum E. L.. ( 1944;). X-ray induced growth factor requirements in bacteria. . Proc Natl Acad Sci U S A 30:, 404–410. [CrossRef].[PubMed].
    [Google Scholar]
  18. Haishima Y., Holst O., Brade H.. ( 1992;). Structural investigation on the lipopolysaccharide of Escherichia coli rough mutant F653 representing the R3 core type. . Eur J Biochem 203:, 127–134. [CrossRef].[PubMed].
    [Google Scholar]
  19. Heinrichs D. E., Yethon J. A., Whitfield C.. ( 1998;). Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. . Mol Microbiol 30:, 221–232. [CrossRef].[PubMed].
    [Google Scholar]
  20. Holst O.. ( 1999;). Chemical structure of the core region of lipopolysaccharides. . In Endotoxins in Health and Disease, pp. 115–154. Edited by Morrison D., Brade H., Opal S., Vogel S... New York:: Marcel Dekker;.
    [Google Scholar]
  21. Holst O., Zähringer U., Brade H., Zamojski A.. ( 1991;). Structural analysis of the heptose/hexose region of the lipopolysaccharide from Escherichia coli K-12 strain W3100. . Carbohydr Res 215:, 323–335. [CrossRef].[PubMed].
    [Google Scholar]
  22. Holst O., Moran A. P., Brennan P. J.. ( 2009;). Microbial Glycobiology. Structures, Relevance and Applications, pp. 3–13. Edited by Moran A. P., Holst O., Brennan P. J., von Itzstein M... Amsterdam:: Academic Press;.
    [Google Scholar]
  23. Jann B., Shashkov A. S., Kochanowski H., Jann K.. ( 1994;). Structure of the O16 polysaccharide from Escherichia coli O16 : K1: an NMR investigation. . Carbohydr Res 264:, 305–311. [CrossRef].[PubMed].
    [Google Scholar]
  24. Jansson P. E., Lindberg A. A., Lindberg B., Wollin R.. ( 1981;). Structural studies on the hexose region of the core in lipopolysaccharides from Enterobacteriaceae. . Eur J Biochem 115:, 571–577. [CrossRef].[PubMed].
    [Google Scholar]
  25. Liu D., Reeves P. R.. ( 1994;). Escherichia coli K12 regains its O antigen. . Microbiology 140:, 49–57. [CrossRef].[PubMed].
    [Google Scholar]
  26. MacLean L. L., Perry M. B.. ( 1997;). Structural characterization of the serotype O : 5 O-polysaccharide antigen of the lipopolysaccharide of Escherichia coli O : 5. . Biochem Cell Biol 75:, 199–205. [CrossRef].[PubMed].
    [Google Scholar]
  27. Margulies M., Egholm M., Altman W. E., Attiya S., Bader J. S., Bemben L. A., Berka J., Braverman M. S., Chen Y. J. et al. ( 2005;). Genome sequencing in microfabricated high-density picolitre reactors. . Nature 437:, 376–380.[PubMed].
    [Google Scholar]
  28. Mullane N., O’Gaora P., Nally J. E., Iversen C., Whyte P., Wall P. G., Fanning S.. ( 2008;). Molecular analysis of the Enterobacter sakazakii O-antigen gene locus. . Appl Environ Microbiol 74:, 3783–3794. [CrossRef].[PubMed].
    [Google Scholar]
  29. Müller-Loennies S., Lindner B., Brade H.. ( 2002;). Structural analysis of deacylated lipopolysaccharide of Escherichia coli strains 2513 (R4 core-type) and F653 (R3 core-type). . Eur J Biochem 269:, 5982–5991. [CrossRef].[PubMed].
    [Google Scholar]
  30. Müller-Loennies S., Lindner B., Brade H.. ( 2003;). Structural analysis of oligosaccharides from lipopolysaccharide (LPS) of Escherichia coli K12 strain W3100 reveals a link between inner and outer core LPS biosynthesis. . J Biol Chem 278:, 34090–34101. [CrossRef].[PubMed].
    [Google Scholar]
  31. Perelle S., Dilasser F., Grout J., Fach P.. ( 2002;). Identification of the O-antigen biosynthesis genes of Escherichia coli O91 and development of a O91 PCR serotyping test. . J Appl Microbiol 93:, 758–764. [CrossRef].[PubMed].
    [Google Scholar]
  32. Petzl W., Zerbe H., Günther J., Yang W., Seyfert H. M., Nürnberg G., Schuberth H. J.. ( 2008;). Escherichia coli, but not Staphylococcus aureus triggers an early increased expression of factors contributing to the innate immune defense in the udder of the cow. . Vet Res 39:, 18. [CrossRef].[PubMed].
    [Google Scholar]
  33. Pföstl A., Zayni S., Hofinger A., Kosma P., Schäffer C., Messner P.. ( 2008;). Biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α-d-glucose. . Biochem J 410:, 187–194. [CrossRef].[PubMed].
    [Google Scholar]
  34. Raetz C. R., Whitfield C.. ( 2002;). Lipopolysaccharide endotoxins. . Annu Rev Biochem 71:, 635–700. [CrossRef].[PubMed].
    [Google Scholar]
  35. Reeves P. P., Wang L.. ( 2002;). Genomic organization of LPS-specific loci. . Curr Top Microbiol Immunol 264:, 109–135.[PubMed].
    [Google Scholar]
  36. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M. A., Barrell B.. ( 2000;). Artemis: sequence visualization and annotation. . Bioinformatics 16:, 944–945. [CrossRef].[PubMed].
    [Google Scholar]
  37. Sadovskaya I., Brisson J. R., Thibault P., Richards J. C., Lam J. S., Altman E.. ( 2000;). Structural characterization of the outer core and the O-chain linkage region of lipopolysaccharide from Pseudomonas aeruginosa serotype O5. . Eur J Biochem 267:, 1640–1650. [CrossRef].[PubMed].
    [Google Scholar]
  38. Samuel G., Reeves P. R. J.. ( 2003;). Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. . Carbohydr Res 338:, 2503–2519. [CrossRef].[PubMed].
    [Google Scholar]
  39. Sawardeker J. S., Sloneker J. H., Jeanes A.. ( 1965;). Quantitative determination of monosaccharides as their alditol acetates by gas liquid chromatography. . Anal Chem 37:, 1602–1604. [CrossRef]
    [Google Scholar]
  40. Stenutz R., Weintraub A., Widmalm G.. ( 2006;). The structures of Escherichia coli O-polysaccharide antigens. . FEMS Microbiol Rev 30:, 382–403. [CrossRef].[PubMed].
    [Google Scholar]
  41. Stevenson G., Neal B., Liu D., Hobbs M., Packer N. H., Batley M., Redmond J. W., Lindquist L., Reeves P.. ( 1994;). Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster. . J Bacteriol 176:, 4144–4156.[PubMed].
    [Google Scholar]
  42. Urbina F., Nordmark E. L., Yang Z., Weintraub A., Scheutz F., Widmalm G.. ( 2005;). Structural elucidation of the O-antigenic polysaccharide from the enteroaggregative Escherichia coli strain 180/C3 and its immunochemical relationship with E. coli O5 and O65. . Carbohydr Res 340:, 645–650. [CrossRef].[PubMed].
    [Google Scholar]
  43. Vinogradov E. V., Van Der Drift K., Thomas-Oates J. E., Meshkov S., Brade H., Holst O.. ( 1999;). The structures of the carbohydrate backbones of the lipopolysaccharides from Escherichia coli rough mutants F470 (R1 core type) and F576 (R2 core type). . Eur J Biochem 261:, 629–639. [CrossRef].[PubMed].
    [Google Scholar]
  44. Wang L., Liu B., Kong Q., Steinrück H., Krause G., Beutin L., Feng L.. ( 2005;). Molecular markers for detection of pathogenic Escherichia coli strains belonging to serogroups O 138 and O 139. . Vet Microbiol 111:, 181–190. [CrossRef].[PubMed].
    [Google Scholar]
  45. 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. [CrossRef].[PubMed].
    [Google Scholar]
  46. Westphal O., Jann K.. ( 1965;). Bacterial lipopolysaccharide extraction with phenol-water and further application of procedure. . Met Carbohydr Chem 5:, 83–87.
    [Google Scholar]
  47. Xiang S. H., Hobbs M., Reeves P. R.. ( 1994;). Molecular analysis of the rfb gene cluster of a group D2 Salmonella enterica strain: evidence for its origin from an insertion sequence-mediated recombination event between group E and D1 strains. . J Bacteriol 176:, 4357–4365.[PubMed].
    [Google Scholar]
  48. Zarrouk H., Karibian D., Godard I., Perry M. B., Caroff M.. ( 1997;). Use of mass spectrometry to compare three O-chain linked and free lipopolysaccharide cores: differences found in Bordetella parapertussis. . J Endotoxin Res 4:, 453–458.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.046912-0
Loading
/content/journal/micro/10.1099/mic.0.046912-0
Loading

Data & Media loading...

Supplements

vol. , part 6, pp. 1750 - 1760

Characteristics of the ORFs located in the O-antigen gene cluster of strain 1303 [ PDF] (66 kb)



PDF
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