Advertisement

Microbiology

, Volume 86, Issue 3, pp 310–316 | Cite as

Effect of O-acetylation of O antigen of Escherichia coli lipopolysaccharide on the nonspecific barrier function of the outer membrane

  • E. E. KulikovEmail author
  • J. Majewska
  • N. S. Prokhorov
  • A. K. Golomidova
  • E. V. Tatarskiy
  • A. V. Letarov
Experimental Articles

Abstract

Comparison of the methods for determination of permeability of the outer membrane of Escherichia coli strain 4s and its mutants was carried out. The studied isogenic strains E. coli 4s were obtained by selection of spontaneous mutants according to their sensitivity to bacteriophages recognizing the surface O antigen of the outer membrane lipopolysaccharide as a primary receptor. The variants differed in the presence and (de)acetylation of the lipopolysaccharide O antigen. A peptide antibiotic polymyxin, plasmid DNA, and lysozyme were used as probes. The role of acetylation of the O antigen of the lipopolysaccaride of E. coli outer membrane in modification of its permeability (correlating with bacteriophage sensitivity of the cells) was confirmed. Kinetic analysis using lysozyme was shown to be the optimal method for determination of the barrier function of E. coli outer membrane.

Keywords

Escherichia coli spontaneous mutants bacteriophage sensitivity lipopolysaccharide O antigen polymyxin lysozyme outer membrane permeability O antigen acetylation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bentley, A.T. and Klebba, P.E, Effect of lipopolysaccharide structure on reactivity of antiporin monoclonal antibodies with the bacterial cell surface, J. Bacteriol., 1988, vol. 170, pp. 1063–1068.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bertani, G, Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli, J. Bacteriol., 1951, vol. 62, pp. 293–300.PubMedPubMedCentralGoogle Scholar
  3. Delcour, A.H, Outer membrane permeability and antibiotic resistance, Biochim. Biophys. Acta, 2009, vol. 1794, pp. 808–816.CrossRefPubMedGoogle Scholar
  4. Domingues, M.M., Inacio, R.G., Raimundo, J.M., Martins, M., Castanho, M.A., and Santos, N.C, Biophysical characterization of polymyxin B interaction with LPS aggregates and membrane model systems, Biopolymers, 2012, vol. 98, pp. 338–344.CrossRefPubMedGoogle Scholar
  5. Fiedler, S. and Wirth, R, Transformation of bacteria with plasmid DNA by electroporation, Anal. Biochem., 1988, vol. 170, pp. 38–44.CrossRefPubMedGoogle Scholar
  6. Golomidova, A.K., Kulikov, E.E., Prokhorov, N.S., Guerrero-Ferreira, R., Knirel, Y.A., Kostryukova, E.S., Tarasyan, K.K., and Letarov A.V, Branched lateral tail fiber organization in T5-like bacteriophages DT57C and DT571/2 is revealed by genetic and functional analysis, Viruses, 2016, vol. 8, no. 1. pii: E26. doi 10.3390/v8010026CrossRefPubMedGoogle Scholar
  7. Graham, G.S., Treick, R.W., and Brunner, D.P, Effect of Ca2+ and Mg2+ upon the reassociation by Escherichia coli of material released by ethylenediaminetetraacetate, Curr. Microbiol., 1979, vol. 2, pp. 339–343.CrossRefGoogle Scholar
  8. Hitchcock, P.J, Analyses of gonococcal lipopolysaccharide in whole-cell lysates by sodium dodecyl sulfate-polyacrylamide gel electrophoresis: stable association of lipopolysaccharide with the major outer membrane protein (protein I) of Neisseria gonorrhoeae, Infect. Immun., 1984, vol. 46, pp. 202–212.PubMedPubMedCentralGoogle Scholar
  9. Irvin, R.T., MacAlister, T.J., and Costerton, J.W, Tris(hydroxymethyl)aminomethane buffer modification of Escherichia coli outer membrane permeability, J. Bacteriol., 1981, vol. 145, pp. 1397–1403.PubMedPubMedCentralGoogle Scholar
  10. Jeworrek, C., Evers, F., Howe, J., Brandenburg, K., Tolan, M., and Winter, R, Effects of specific versus nonspecific ionic interactions on the structure and lateral organization of lipopolysaccharides, Biophys. J., 2011, vol. 100, pp. 2169–2177.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Kimura, Y., Matsunaga, H., and Vaara, M, Polymyxin B octapeptide and polymyxin B heptapeptide are potent outer membrane permeability-increasing agents, J. Antibiot. (Tokyo), 1992, vol. 45, pp. 742–749.CrossRefGoogle Scholar
  12. Knirel, Y.A., Prokhorov, N.S., Shashkov, A.S., Ovchinnikova, O.G., Zdorovenko, E.L., Liu, B., Kostryukova, E.S., Larin, A.K., Golomidova, A.K., and Letarov, A.V, Variations in O-antigen biosynthesis and O-acetylation associated with altered phage sensitivity in Escherichia coli 4s, J. Bacteriol., 2015, vol. 197, pp. 905–912.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kulikov, E., Kropinski, A.M., Golomidova, A., Lingohr, E., Govorun, V., Serebryakova, M., Prokhorov, N., Letarova, M., Manykin, A., Strotskaya, A., and Letarov, A, Isolation and characterization of a novel indigenous intestinal N4-related coliphage vB_EcoP_G7C, Virology, 2012, vol. 426, pp. 93–99.CrossRefPubMedGoogle Scholar
  14. Lineweaver, H. and Burk, D, The determination of enzyme dissociation constants, J. Amer. Chem. Soc., 1934, vol. 56, pp. 658–666.CrossRefGoogle Scholar
  15. MacLachlan, P.R. and Sanderson, K.E, Transformation of Salmonella typhimurium with plasmid DNA: differences between rough and smooth strains, J. Bacteriol., 1985, vol. 161, pp. 442–445.PubMedPubMedCentralGoogle Scholar
  16. Morrison, D.C. and Jacobs, D.M, Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides, Immunochem., 1976, vol. 13, pp. 813–818.CrossRefGoogle Scholar
  17. Nicas, T.I. and Hancock, R.E, Alteration of susceptibility to EDTA,polymyxin B and gentamicin in Pseudomonas aeruginosa by divalent cation regulation of outer membrane protein H1, J. Gen. Microbiol., 1983, vol. 129, pp. 509–517.PubMedGoogle Scholar
  18. Repaske, R, Lysis of gram-negative bacteria by lysozyme, Biochim. Biophys. Acta, 1956, vol. 22, pp. 189–191.CrossRefPubMedGoogle Scholar
  19. Repaske, R, Lysis of gram-negative organisms and the role of versene, Biochim. Biophys. Acta, 1958, vol. 30, pp. 225–232.CrossRefPubMedGoogle Scholar
  20. Rocque, W.J., Coughlin, R.T., and McGroarty, E.J, Lipopolysaccharide tightly bound to porin monomers and trimers from Escherichia coli K-12, J. Bacteriol., 1987, vol. 169, pp. 4003–4010.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Seed K.D, Battling phages: how bacteria defend against viral attack, PLoS Pathog., 2015, vol. 11, p. e1004847.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Sherbet, G.V. and Lakshmi, M.S, Characterisation of Escherichia coli cell surface by isoelectric equilibrium analysis, Biochim. Biophys. Acta, 1973, vol. 298, pp. 50–58.CrossRefPubMedGoogle Scholar
  23. Silhavy, T.J., Kahne, D., and Walker, S, The bacterial cell envelope, Cold Spring Harb. Perspect. Biol., 2010, vol. 2, p. a000414.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Singh, A. and Reithmeier, R, Leakage of periplasmic enzymes from cells of heptose-deficient mutants of Escherichia coli, associated with alterations in the protein component of the outer membrane, J. Gen. Appl. Microbiol., 1975, vol. 21, pp. 109–118.Google Scholar
  25. Tsai, C.M. and Frasch, C.E., A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels, Anal. Biochem., 1982, vol. 119, pp. 115–119.Google Scholar
  26. Tsuchido, T., Katsui, N., Takeuchi, A., Takano, M., and Shibasaki, I, Destruction of the outer membrane permeability barrier of Escherichia coli by heat treatment, Appl. Environ. Microbiol., 1985, vol. 50, pp. 298–303.PubMedPubMedCentralGoogle Scholar
  27. Tu, Q., Yin, J., Fu, J., Herrmann, J., Li, Y., Yin, Y., Stewart, A.F., Muller, R., and Zhang, Y., Room temperature electrocompetent bacterial cells improve DNA transformation and recombineering efficiency, Sci. Rep., 2016, vol. 6, P. 24648. doi 10.1038/srep24648CrossRefPubMedPubMedCentralGoogle Scholar
  28. Tytgat, H.L. and Lebeer, S, The sweet tooth of bacteria: common themes in bacterial glycoconjugates, Microbiol. Mol. Biol. Rev., 2014, vol. 78, pp. 372–417.CrossRefPubMedPubMedCentralGoogle Scholar
  29. van der Woude, M.W, Phase variation: how to create and coordinate population diversity, Curr. Opin. Microbiol., 2011, vol. 14, pp. 205–211.CrossRefPubMedGoogle Scholar
  30. van der Woude, M.W. and Baumler, A.J, Phase and antigenic variation in bacteria, Clin. Microbiol. Rev., 2004, vol. 17, pp. 581–611.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Verkleij, A., van Alphen, L., Bijvelt, J., and Lugtenberg, B, Architecture of the outer membrane of Escherichia coli K12. II. Freeze fracture morphology of wild type and mutant strains, Biochim. Biophys. Acta, 1977, vol. 466, pp. 269–282.CrossRefPubMedGoogle Scholar
  32. Wiegand, I., Hilpert, K., and Hancock, R.E, Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances, Nat. Protoc., 2008, vol. 3, pp. 163–175.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • E. E. Kulikov
    • 1
    Email author
  • J. Majewska
    • 2
  • N. S. Prokhorov
    • 1
  • A. K. Golomidova
    • 1
  • E. V. Tatarskiy
    • 1
  • A. V. Letarov
    • 1
  1. 1.Winogradsky Institute of Microbiology, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  2. 2.Hirszfeld Institute of Immunology and Experimental TherapyPolish Academy of SciencesPolishPoland

Personalised recommendations