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Structural relationships between genetically closely related O-antigens of Escherichia coli and Shigella spp.

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An Erratum to this article was published on 15 November 2018

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Abstract

Gene clusters for biosynthesis of 24 of 34 basic O-antigen forms of Shigella spp. are identical or similar to those of the genetically closely related bacterium Escherichia coli. For 18 of these relatedness was confirmed chemically by elucidation of the O-antigen (O-polysaccharide) structures. In this work, structures of the six remaining O-antigens of E. coli O32, O53, O79, O105, O183 (all related to S. boydii serotypes), and O38 (related to S. dysenteriae type 8) were established using 1H and 13C NMR spectroscopy. They were found to be identical to the Shigella counterparts, except for the O32- and O38-polysaccharides, which differ in the presence of O-acetyl groups. The structure of the E. coli O105-related O-polysaccharide of S. boydii type 11 proposed earlier is revised. The contents of the O-antigen gene clusters of the related strains of E. coli and Shigella spp. and different mechanisms of O-antigen diversification in these bacteria are discussed in view of the O-polysaccharide structures established. These data illustrate the value of the O-antigen chemistry and genetics for elucidation of evolutionary relationships of bacteria.

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Change history

  • 15 November 2018

    Errors have been found in polysaccharide structures on pages 603 (Fig. 3), 606 (Figs. 13-15) and 607 (Fig. 17). The following are the correct structures.

Abbreviations

COSY:

correlation spectroscopy

Cro-2-P :

glyc-erol 2-phosphate

GalNAc:

2-acetamido-2-deoxygalactose

GlcA:

glucuronic acid GlcNAc, 2-acetamido-2-deoxyglu-cose

HMBC:

heteronuclear multiple-bond correlation

HSQC:

heteronuclear single-quantum coherence

Rha:

rham-nose

Rlac:

(R)-1-carboxyethyl (lactic acid ether)

ROESY:

rotating-frame nuclear Overhauser effect spectroscopy

Rpyr:

(R)-1-carboxyethylidene (pyruvic acid acetal)

TOCSY:

total correlation spectroscopy

References

  1. Pupo, G. M., Lan, R., and Reeves, P. R. (2000) Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics, Proc. Natl. Acad. Sci. USA, 97, 10567–10572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Knirel, Y. A., Sun, Q., Senchenkova, S. N., Lan, R., Perepelov, A. V., and Xu, J. (2015) O-Antigen modifications providing the antigenic diversity of Shigella flexneri and the underlying genetic mechanisms, Biochemistry (Moscow), 80, 901–914.

    Article  CAS  Google Scholar 

  3. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins, Annu. Rev. Biochem., 71, 635–700.

    Article  CAS  PubMed  Google Scholar 

  4. Liu, B., Knirel, Y. A., Feng, L., Perepelov, A. V., Senchenkova, S. N., Wang, Q., Reeves, P. R., and Wang, L. (2008) Structure and genetics of Shigella O-antigens, FEMS Microbiol. Rev., 32, 627–653. Corrigendum: (2010) FEMS Microbiol. Rev., 34, 606.

    Article  PubMed  Google Scholar 

  5. Iguchi, A., Iyoda, S., Kikuchi, T., Ogura, Y., Katsura, K., Ohnishi, M., Hayashi, T., and Thomson, N. R. (2014) A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster, DNA Res., 22, 105107.

    Google Scholar 

  6. Perepelov, A. V., Shevelev, S. D., Liu, B., Senchenkova, S. N., Shashkov, A. S., Feng, L., Knirel, Y. A., and Wang, L. (2010) Structures of the O-antigens of Escherichia coli O13, O129 and O135 related to the O-antigens of Shigella flexneri, Carbohydr. Res., 345, 1594–1599.

    CAS  PubMed  Google Scholar 

  7. Perepelov, A. V., Shashkov, A. S., Guo, X., Filatov, A. V., Weintraub, A., Widmalm, G., and Knirel, Y. A. (2015) Structure and genetics of the O-antigen of Escherichia coli O169 related to the O-antigen of Shigella boydii type 6, Carbohydr. Res., 414, 46–50.

    Article  CAS  PubMed  Google Scholar 

  8. Robbins, P. W., and Uchida, T. (1962) Studies on the chemical basis of the phage conversion of O-antigens in the Egroup Salmonellae, Biochemistry, 1, 323–335.

    Article  CAS  PubMed  Google Scholar 

  9. Westphal, O., and Jann, K. (1965) Bacterial lipopolysaccharides. Extraction with phenol–water and further applications of the procedure, Methods Carbohydr. Chem., 5, 83–91.

    CAS  Google Scholar 

  10. Lipkind, G. M., Shashkov, A. S., Knirel, Y. A., Vinogradov, E. V., and 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.

    Article  CAS  PubMed  Google Scholar 

  11. Perepelov, A. V., Senchenkova, S. N., Shashkov, A. S., Liu, B., Feng, L., Wang, L., and Knirel, Y. A. (2008) Antigenic polysaccharides of bacteria. 40. Revision of the structures of the O-specific polysaccharides of Shigella dysenteriae types 3, 9. and Shigella boydii type 4 by NMR spectroscopy, Russ. J. Bioorg. Chem., 34, 110–117.

    Article  CAS  Google Scholar 

  12. L’vov, V. L., Shashkov, A. S., Knirel, Y. A., Arifulina, A. E., Senchenkova, S. N., Yakovlev, A. V., and Dmitriev, B. A. (1995) Structure of the O-specific polysaccharide chain of Shigella boydii type 5 lipopolysaccharide: a repeated study, Carbohydr. Res., 279, 183–192.

    Article  PubMed  Google Scholar 

  13. Senchenkova, S. N., Feng, L., Yang, J., Shashkov, A. S., Cheng, J., Liu, D., Knirel, Y. A., Reeves, P., Jin, Q., Ye, Q., and Wang, L. (2005) Structural and genetic characterization of the Shigella boydii type 10 and type 6 O-antigens, J. Bacteriol., 187, 2551–2554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. L’vov, V. L., Yakovlev, A. V., Shashkov, A. S., and Dmitriev, B. A. (1991) Antigenic polysaccharides of bacteria. The structure of the polysaccharide chain of the lipopolysaccharide of Shigella boydii type 11, Bioorg. Khim., 17, 111–120.

    PubMed  Google Scholar 

  15. Perepelov, A. V., Senchenkova, S. N., Shashkov, A. S., Knirel, Y. A., Liu, B., Feng, L., and Wang, L. (2008) Antigenic polysaccharides of bacteria. 42. Structures of the O-polysaccharides from two Shigella dysenteriae type 8 strains, Russ. J. Bioorg. Chem., 34, 725–729.

    Article  CAS  Google Scholar 

  16. L’vov, V. L., Yakovlev, A. V., Pluzhnikova, G. N., Lapina, E. B., Shashkov, A. S., and Dmitriev, B. A. (1987) Antigenic polysaccharides of bacteria. The structure of the polysaccharide chain of the Shigella boydii type 14 lipopolysaccharide, Bioorg. Khim., 13, 1256–1265.

    PubMed  Google Scholar 

  17. Shepherd, J. G., Wang, L., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, 119991, Moscow, Russia

    Y. A. Knirel, A. S. Shashkov, O. V. Sizova, E. L. Zdorovenko, O. I. Naumenko, S. N. Senchenkova & A. V. Perepelov

  2. Nankai University, TEDA Institute of Biological Sciences and Biotechnology, Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, 300457, Tianjin, China

    Chengqian Qian & Bin Liu

Authors
  1. Y. A. Knirel
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  2. Chengqian Qian
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  3. A. S. Shashkov
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  4. O. V. Sizova
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  5. E. L. Zdorovenko
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  6. O. I. Naumenko
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  7. S. N. Senchenkova
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  8. A. V. Perepelov
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  9. Bin Liu
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Corresponding author

Correspondence to Y. A. Knirel.

Additional information

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM16-028, April 3, 2016.

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Knirel, Y.A., Qian, C., Shashkov, A.S. et al. Structural relationships between genetically closely related O-antigens of Escherichia coli and Shigella spp.. Biochemistry Moscow 81, 600–608 (2016). https://doi.org/10.1134/S0006297916060067

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  • DOI: https://doi.org/10.1134/S0006297916060067

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