Biochemistry (Moscow)

, Volume 81, Issue 6, pp 600–608 | Cite as

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

  • Y. A. KnirelEmail author
  • Chengqian Qian
  • A. S. Shashkov
  • O. V. Sizova
  • E. L. Zdorovenko
  • O. I. Naumenko
  • S. N. Senchenkova
  • A. V. Perepelov
  • Bin Liu


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.

Key words

Escherichia coli Shigella dysenteriae Shigella boydii O-polysaccharide structure O-antigen gene cluster 



correlation spectroscopy


glyc-erol 2-phosphate




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


heteronuclear multiple-bond correlation


heteronuclear single-quantum coherence




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


rotating-frame nuclear Overhauser effect spectroscopy


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


total correlation spectroscopy


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 3.
    Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins, Annu. Rev. Biochem., 71, 635–700.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. 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. 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.PubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.Google Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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.PubMedGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. 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.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • Y. A. Knirel
    • 1
    Email author
  • Chengqian Qian
    • 2
  • A. S. Shashkov
    • 1
  • O. V. Sizova
    • 1
  • E. L. Zdorovenko
    • 1
  • O. I. Naumenko
    • 1
  • S. N. Senchenkova
    • 1
  • A. V. Perepelov
    • 1
  • Bin Liu
    • 2
  1. 1.Zelinsky Institute of Organic ChemistryRussian Academy of SciencesMoscowRussia
  2. 2.Nankai University, TEDA Institute of Biological Sciences and BiotechnologyKey Laboratory of Molecular Microbiology and Technology, Ministry of EducationTianjinChina

Personalised recommendations