The O-polysaccharide of Escherichia coli F5, which is structurally related to that of E. coli O28ab, provides cells only weak protection against bacteriophage attack

  • A. K. Golomidova
  • O. I. Naumenko
  • S. N. Senchenkova
  • Y. A. Knirel
  • A. V. LetarovEmail author
Brief Report


Several types of Escherichia coli O-antigens form highly effective shields protecting the bacterial cell surface and preventing bacteriophages from interacting directly with their secondary (terminal) receptors. However, it is not clear if O-antigens of various types (O-serotypes) differ in their anti-phage protection efficacy. Here, we describe a new E. coli strain, F5, which has an E. coli O28ab-related O-antigen. Although the amount of O-antigen produced by this strain is comparable to that produced by other E. coli strains we tested, it appears to give the cells significantly lower protection against phage attack than other O-antigen types, such as the O-polysaccharide of E. coli F17, which we studied earlier.



The authors thank Dr. A.S. Dmitrenok and Prof. A.S. Shashkov for help with NMR spectroscopy, and Dr. A.O. Chizhov for measuring the mass spectrum. We are also grateful to Dr. Ember Johnson-Neuroth from The Evergreen State College, USA, for the linguistic correction of the manuscript. This work was supported partially by the Russian Science Foundation Grant no. 15-15-00134P (structural analysis of the O-antigen and screening of environmental objects).

Supplementary material

705_2019_4371_MOESM1_ESM.docx (487 kb)
Supplementary material 1 (DOCX 486 kb)


  1. 1.
    Kulikov E, Majewska J, Prokhorov N, Golomidova A, Tatarskiy E, Letarov A (2017) Effect of O-acetylation of O antigen of Escherichia coli lipopolysaccharide on the nonspecific barrier function of the outer membrane. Microbiology 86(3):310–316CrossRefGoogle Scholar
  2. 2.
    Coggon CF, Jiang A, Goh KGK, Henderson IR, Schembri MA, Wells TJ (2018) A novel method of serum resistance by Escherichia coli that causes urosepsis. mBio 9:3. CrossRefGoogle Scholar
  3. 3.
    Zivanovic Y, Confalonieri F, Ponchon L, Lurz R, Chami M, Flayhan A, Renouard M, Huet A, Decottignies P, Davidson AR, Breyton C, Boulanger P (2014) Insights into bacteriophage T5 structure from analysis of its morphogenesis genes and protein components. J Virol 88(2):1162–1174. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Osawa K, Shigemura K, Iguchi A, Shirai H, Imayama T, Seto K, Raharjo D, Fujisawa M, Osawa R, Shirakawa T (2013) Modulation of O-antigen chain length by the wzz gene in Escherichia coli O157 influences its sensitivities to serum complement. Microbiol Immunol 57(9):616–623. CrossRefPubMedGoogle Scholar
  5. 5.
    Sharp C, Boinett C, Cain A, Housden N, Kumar S, Turner K, Parkhill J, Kleanthous C (2018) O-antigen dependent colicin insensitivity of uropathogenic Escherichia coli. J Bacteriol. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Knirel YA, Prokhorov NS, Shashkov AS, Ovchinnikova OG, Zdorovenko EL, Liu B, Kostryukova ES, Larin AK, Golomidova AK, Letarov AV (2015) Variations in O-antigen biosynthesis and O-acetylation associated with altered phage sensitivity in Escherichia coli 4s. J Bacteriol 197(5):905–912. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Golomidova AK, Kulikov EE, Prokhorov NS, Guerrero-Ferreira Rcapital Es C, Knirel YA, Kostryukova ES, Tarasyan KK, Letarov AV (2016) Branched lateral tail fiber organization in T5-like bacteriophages DT57C and DT571/2 is revealed by genetic and functional analysis. Viruses 8:1. CrossRefGoogle Scholar
  8. 8.
    Letarov AV, Kulikov EE (2018) Determination of the bacteriophage host range: culture-based approach. Methods Mol Biol 1693:75–84. CrossRefPubMedGoogle Scholar
  9. 9.
    Broeker NK, Barbirz S (2017) Not a barrier but a key: How bacteriophages exploit host’s O-antigen as an essential receptor to initiate infection. Mol Microbiol 105(3):353–357. CrossRefPubMedGoogle Scholar
  10. 10.
    Broeker NK, Kiele F, Casjens SR, Gilcrease EB, Thalhammer A, Koetz J, Barbirz S (2018) In vitro studies of lipopolysaccharide-mediated DNA release of Podovirus HK620. Viruses 10:6. CrossRefGoogle Scholar
  11. 11.
    Kulikov EE, Golomidova AK, Prokhorov NS, Ivanov PA, Letarov AV (2019) High-throughput LPS profiling as a tool for revealing of bacteriophage infection strategies. Sci Rep 9(1):2958. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Heller K, Braun V (1982) Polymannose O-antigens of Escherichia coli, the binding sites for the reversible adsorption of bacteriophage T5+ via the L-shaped tail fibers. J Virol 41(1):222–227PubMedPubMedCentralGoogle Scholar
  13. 13.
    Knirel YA, Ivanov PA, Senchenkova SN, Naumenko OI, Ovchinnikova OO, Shashkov AS, Golomidova AK, Babenko VV, Kulikov EE, Letarov AV (2019) Structure and gene cluster of the O antigen of Escherichia coli F17, a candidate for a new O-serogroup. Int J Biol Macromol 124:389–395. CrossRefPubMedGoogle Scholar
  14. 14.
    Kulikov EE, Golomidova AK, Letarova MA, Kostryukova ES, Zelenin AS, Prokhorov NS, Letarov AV (2014) Genomic sequencing and biological characteristics of a novel Escherichia coli bacteriophage 9g, a putative representative of a new Siphoviridae genus. Viruses 6(12):5077–5092. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Thiaville JJ, Kellner SM, Yuan Y, Hutinet G, Thiaville PC, Jumpathong W, Mohapatra S, Brochier-Armanet C, Letarov AV, Hillebrand R, Malik CK, Rizzo CJ, Dedon PC, de Crecy-Lagard V (2016) Novel genomic island modifies DNA with 7-deazaguanine derivatives. Proc Natl Acad Sci USA 113(11):E1452–E1459. CrossRefPubMedGoogle Scholar
  16. 16.
    Tsai R, Correa IR, Xu MY, Xu SY (2017) Restriction and modification of deoxyarchaeosine (dG(+))-containing phage 9 g DNA. Sci Rep 7(1):8348. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Golomidova AK, Kulikov EE, Babenko VV, Ivanov PA, Prokhorov NS, Letarov AV (2018) Escherichia coli bacteriophage Gostya9, representing a new species within the genus T5virus. Arch Virol. CrossRefPubMedGoogle Scholar
  18. 18.
    Lipkind GM, Shashkov AS, Knirel YA, Vinogradov EV, Kochetkov NK (1988) A computer-assisted structural analysis of regular polysaccharides on the basis of 13C-NMR data. Carbohyd Res 175(1):59–75CrossRefGoogle Scholar
  19. 19.
    Shashkov AS, Yang B, Senchenkova SN, Perepelov AV, Liu B, Knirel YA (2016) Structures and genetics of biosynthesis of glycerol 1-phosphate-containing O-polysaccharides of Escherichia coli O28ab, O37, and O100. Carbohyd Res 426:26–32. CrossRefGoogle Scholar
  20. 20.
    Zdorovenko EL, Wang Y, Shashkov AS, Chen T, Ovchinnikova OG, Liu B, Golomidova AK, Babenko VV, Letarov AV, Knirel YA (2018) O-Antigens of Escherichia coli strains O81 and HS3-104 are structurally and genetically related, except O-antigen glucosylation in E. coli HS3-104. Biochem Biokhim 83(5):534–541. CrossRefGoogle Scholar
  21. 21.
    Zdorovenko EL, Golomidova AK, Prokhorov NS, Shashkov AS, Wang L, Letarov AV, Knirel YA (2015) Structure of the O-polysaccharide of Escherichia coli O87. Carbohyd Res 412:15–18. CrossRefGoogle Scholar
  22. 22.
    Golomidova AK, Kulikov EE, Babenko VV, Kostryukova ES, Letarov AV (2018) Complete genome sequence of bacteriophage St11Ph5, which Infects uropathogenic Escherichia coli strain up11. Genome Announc 6:2. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.S. N. Winogradsky Institute of Microbiology, Federal Research Centre, “Fundamentals of Biotechnology”, Russian Academy of SciencesMoscowRussian Federation
  2. 2.N. D. Zelinsky Institute of Organic Chemistry, Russian Academy of SciencesMoscowRussian Federation
  3. 3.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussian Federation

Personalised recommendations