Genetic characterisation and structural analysis of the O-specific polysaccharide of Yersinia pseudotuberculosis serotype O:1c

Abstract

Many, but not all, of the current 21 serotypes of Yersinia pseudotuberculosis have been investigated with regard to the chemical structures of their O-specific polysaccharide (OPS) and the genetic basis of their biosynthesis. Completion of the genetics and structures of the remaining serotypes will enhance our understanding of the emerging relationship between genetics and structures within this species. Here, we present a structural and genetic analysis of the Y. pseudotuberculosis serotype O:1c OPS. Our results showed that this OPS has the same backbone as Y. pseudotuberculosis O:2b, but with a 3,6-dideoxy-D-ribo-hexofuranose (paratofuranose, Parf) side-branch instead of a 3,6-dideoxy-D-xylo-hexopyranose (abequopyranose, Abep). The 3^'-end of the gene cluster is the same as for O:2b and has the genes for synthesis of the backbone and for processing the completed repeat unit. The 5^'-end of the cluster consists of the same genes as O:1b for synthesis of Parf and a related gene for its transfer to the repeating unit backbone.

Keywords

Biosynthetic gene cluster D-paratofuranose O-specific polysaccharide O-antigen structure Yersinia pseudotuberculosis

References

Bogdanovich T. , Carniel E. , Fukushima H. , Skurnik M. Use of O-antigen gene cluster-specific PCRs for the identification and O genotyping of Yersinia pseudotuberculosis and Yersinia pestis. J Clin Microbiol 2003; 41: 5103-5112.

Tsubokura M. , Aleksic S. A simplified antigenic scheme for serotyping of Yersinia pseudotuberculosis: phenotypic characterization of reference strains and preparation of O and H factor sera. Contrib Microbiol Immunol 1995; 13: 99-105.

Tsubokura M. , Otsuki K. , Sato K. et al. Special features of distribution of Yersinia pseudotuberculosis in Japan. J Clin Microbiol 1989; 27: 790-791.

Aleksic S. , Bockemuhl J. , Wuthe H. Epidemiology of Yersinia pseudotuberculosis in Germany, 1983-1993. Contrib Microbiol Immunol 1995; 13: 55-58.

Hobbs M. , Reeves PR The JUMPStart sequence: a 39 bp element common to several polysaccharide gene clusters. Mol Microbiol 1994; 12: 855-856.

Reeves PR , Pacinelli E. , Wang L. O-antigen gene clusters of Yersinia pseudotuberculosis. In: Skurnik M , Bengoechea JA , Granfors K. (eds) The Genus Yersinia: Entering the functional genomics era, Kluwer Plenum, 2003; 199-206.

Samuel G. , Reeves PR Biosynthesis of O antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res 2003; 338: 2503-2519.

Thorson JS , Liu HW Characterization of the first PMP-dependent iron-sulfur-containing enzyme which is essential for the biosynthesis of 3,6-dideoxyhexoses. J Am Chem Soc 1993; 115: 7539-7540.

Thorson JS , Lo SF , Liu HW Molecular basis of 3,6-dideoxyhexose biosynthesis: elucidation of CDP-ascarylose biosynthetic genes and their relationship to other 3,6-dideoxyhexose pathways . J Am Chem Soc 1993; 115: 5827-5828.

10.

Thorson JS , Lo SF , Liu HW , Hutchinson CR Biosynthesis of 3,6-dideoxyhexoses: new mechanistic reflections upon 2,6-dideoxy, 4,6-dideoxy, and amino sugar construction. J Am Chem Soc 1993; 115: 6993-6994.

11.

Thorson JS , Lo SF , Ploux O. , He X. , Liu HW Studies of the biosynthesis of 3,6-dideoxyhexoses: molecular cloning and characterization of the asc (ascarylose) region from Yersinia pseudotuberculosis serogroup VA. J Bacteriol 1994; 176: 5483-5493.

12.

Cunneen M. , De Castro C. , Kenyon J. et al. The O-specific polysaccharide structure and biosynthetic gene cluster of Yersinia pseudotuberculosis serotype O:11. Carbohydr Res 2009; 344: 1533-1540.

13.

Kondakova AN , Bystrova OV , Shaikhutdinova RZ et al. Structure of the O antigen of Yersinia pseudotuberculosis O:4b. Carbohydr Res 2009; 344: 152-154.

14.

Kondakova AN , Bystrova OV , Shaikhutdinova RZ et al. Structure of the O antigen of Yersinia pseudotuberculosis O:4a revised. Carbohydr Res 2009; 344: 531-534.

15.

Kondakova AN , Bystrova OV , Shaikhutdinova RZ et al. Structure of the O-polysaccharide of Yersinia pseudotuberculosis O:2b. Carbohydr Res 2009; 344: 405-407.

16.

Kondakova AN , Ho N. , Bystrova OV et al. Structural studies of the O antigens of Yersinia pseudotuberculosis O:2a and mutants thereof with impaired 6-deoxy-D-manno-heptose biosynthesis pathway. Carbohydr Res 2008; 343: 1383-1389.

17.

Kondakova AN , Shaikhutdinova RZ , Ivanov SA et al. Revision of the O-polysaccharide structure of Yersinia pseudotuberculosis O:1b. Carbohydr Res 2009; 344: 2421-2423.

18.

Fukushima H. , Matsuda Y. , Seki R. et al. Geographical heterogeneity between Far Eastern and Western countries in prevalence of the virulence plasmid, the superantigen Yersinia pseudotuberculosis-derived mitogen, and the high-pathogenicity island among Yersinia pseudotuberculosis strains. J Clin Microbiol 2001; 39: 3541-3547.

19.

Nagano T. , Kiyohara T. , Suzuki K. , Tsubokura M. , Otsuki K. Identification of pathogenic strains within serogroups of Yersinia pseudotuberculosis and the presence of non-pathogenic strains isolated from animals and the environment . J Vet Med Sci 1997; 59: 153-158.

20.

Skurnik M. , Peippo A. , Ervela E. Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol Microbiol 2000; 37: 316-330.

21.

De Castro C. , Skurnik M. , Molinaro A. , Holst O. Characterization of the O-polysaccharide structure and biosynthetic gene cluster of Yersinia pseudotuberculosis serotype O:15. Innate Immun 2009; 15: 351-359.

22.

Westphal O. , Jann K. Bacterial lipopolysaccharides. Extraction with phenol-water and further applications of the procedure. In: Whistler RL. (ed.) Methods in Carbohydrate Chemistry. New York: Academic Press, 1965; 83-91.

23.

Oertelt C. , Lindner B. , Skurnik M. , Holst O. Isolation and structural characterization of an R-form lipopolysaccharide from Yersinia enterocolitica serotype O:8. Eur J Biochem 2001; 268: 554-564.

24.

Kamerling JP , Gerwig GJ Strategies for the structural analysis of carbohydrates. In: Lee YC , Boons GJ , Suzuki A , Taniguchi N , Voragen AG. (eds) Comprehensive Glycoscience, from Chemistry to Systems Biology. Oxford: Elsevier, 2007; 1-68.

25.

Leontein K. , Lindberg B. , Lönngren J. Assignment of absolute configuration of sugars by G.L.C. of their acetylated glycosides formed from chiral alcohols. Carbohydr Res 1978; 62: 359-362.

26.

Ciucanu I. , Kerek F. Rapid and simultaneous methylation of fatty and hydroxy fatty acids for gas-liquid chromatographic analysis. J Chromatogr 1984 ; 284: 179-185.

27.

Kjaer M. , Andersen KV , Poulsen FM Automated and semiautomated analysis of homo- and heteronuclear multidimensional nuclear magnetic resonance spectra of proteins: the program Pronto. Methods Enzymol 1994; 239: 288-307.

28.

Maloy SR Experimental techniques in bacterial genetics. Boston, MA: Jones and Bartlett, 1990. p 63.

29.

Gordon D. , Abajian C. , Green P. CONSED - A graphical tool for sequence finishing. Genome Res 1998; 8: 195-202.

30.

Altschul SF , Gish W. , Miller W. , Myers EW , Lipman DJ Basic local alignment search tool. J Mol Biol 1990; 215: 403-410.

31.

Carver TJ , Rutherford KM , Berriman M. , Rajandream MA , Barrell BG , Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics 2005; 21: 3422-3423.

32.

Isakov VV , Gorshkova RP , Tomshich V. , Ovodov Y. 13C-NMR analysis of O-specific side chain polysaccharide of lipopolysaccharide from Yersinia pseudotuberculosis 1B serovar. Bioorganicheskaja Khimija, 1981; 7: 559-562.

33.

Bock K. , Pedersen C. Carbon-13 nuclear magnetic resonance spectroscopy of monosaccharides. Adv Carbohydr Chem Biochem 1983; 41: 27-65.

34.

Reeves PR , Hobbs M. , Valvano M. et al. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol 1996; 4: 495-503.

35.

Pacinelli E. , Wang L. , Reeves PR Relationship of Yersinia pseudotuberculosis O antigens IA, IIA and IVB: The IIA gene cluster was derived from that of IVB. Infect Immun 2002; 70: 3271-3276.

36.

Matero P. , Pasanen T. , Laukkanen R. et al. Real-time multiplex PCR assay for detection of Yersinia pestis and Yersinia pseudotuberculosis. APMIS 2009 ; 117: 34-44.