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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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.
Bertani, G, Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli, J. Bacteriol., 1951, vol. 62, pp. 293–300.
Delcour, A.H, Outer membrane permeability and antibiotic resistance, Biochim. Biophys. Acta, 2009, vol. 1794, pp. 808–816.
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.
Fiedler, S. and Wirth, R, Transformation of bacteria with plasmid DNA by electroporation, Anal. Biochem., 1988, vol. 170, pp. 38–44.
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/v8010026
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.
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.
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.
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.
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.
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.
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.
Lineweaver, H. and Burk, D, The determination of enzyme dissociation constants, J. Amer. Chem. Soc., 1934, vol. 56, pp. 658–666.
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.
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.
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.
Repaske, R, Lysis of gram-negative bacteria by lysozyme, Biochim. Biophys. Acta, 1956, vol. 22, pp. 189–191.
Repaske, R, Lysis of gram-negative organisms and the role of versene, Biochim. Biophys. Acta, 1958, vol. 30, pp. 225–232.
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.
Seed K.D, Battling phages: how bacteria defend against viral attack, PLoS Pathog., 2015, vol. 11, p. e1004847.
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.
Silhavy, T.J., Kahne, D., and Walker, S, The bacterial cell envelope, Cold Spring Harb. Perspect. Biol., 2010, vol. 2, p. a000414.
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.
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.
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.
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/srep24648
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.
van der Woude, M.W, Phase variation: how to create and coordinate population diversity, Curr. Opin. Microbiol., 2011, vol. 14, pp. 205–211.
van der Woude, M.W. and Baumler, A.J, Phase and antigenic variation in bacteria, Clin. Microbiol. Rev., 2004, vol. 17, pp. 581–611.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © E.E. Kulikov, J. Majewska, N.S. Prokhorov, A.K. Golomidova, E.V. Tatarskiy, A.V. Letarov, 2017, published in Mikrobiologiya, 2017, Vol. 86, No. 3, pp. 284–291.
Rights and permissions
About this article
Cite this article
Kulikov, E.E., Majewska, J., Prokhorov, N.S. et al. Effect of O-acetylation of O antigen of Escherichia coli lipopolysaccharide on the nonspecific barrier function of the outer membrane. Microbiology 86, 310–316 (2017). https://doi.org/10.1134/S0026261717030080
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261717030080