1887

Abstract

Colicin release provides producer strains with a competitive advantage under certain circumstances. We found that propagation of M13 bacteriophage in cells producing colicin E7 is impaired, without alteration in the efficiency of bacteriophage adsorption, as compared with non-producing cells. In contrast to the protective effect of the colicin against M13 bacteriophage infection, the endogenously expressed colicin does not confer limited protection against transfection with M13 bacteriophage DNA. Furthermore, it was found that the translocation-receptor-binding domain and toxicity domain of the colicin are able to interact with the M13 major coat protein, g8p, during bacteriophage infection. Based on these observations, we propose that interaction between colicin E7 and g8p during infection interferes with g8p depolymerizing into the cytoplasmic membrane during bacteriophage DNA penetration, thus resulting in the limited protection against M13 bacteriophage infection.

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2010-11-01
2019-11-21
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References

  1. Bannister, D. & Glover, S. W. ( 1968; ). Restriction and modification of bacteriophages by R+ strains of Escherichia coli K12. Biochem Biophys Res Commun 30, 735–738.[CrossRef]
    [Google Scholar]
  2. Cascales, E., Buchanan, S. K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., Riley, M., Slatin, S. & Cavard, D. ( 2007; ). Colicin biology. Microbiol Mol Biol Rev 71, 158–229.[CrossRef]
    [Google Scholar]
  3. Click, E. M. & Webster, R. E. ( 1997; ). Filamentous phage infection: required interactions with the TolA protein. J Bacteriol 179, 6464–6471.
    [Google Scholar]
  4. Click, E. M. & Webster, R. E. ( 1998; ). The TolQRA proteins are required for membrane insertion of the major capsid protein of the filamentous phage f1 during infection. J Bacteriol 180, 1723–1728.
    [Google Scholar]
  5. Coffey, A. & Ross, R. P. ( 2002; ). Bacteriophage-resistance systems in dairy starter strains: molecular analysis to application. Antonie van Leeuwenhoek 82, 303–321.[CrossRef]
    [Google Scholar]
  6. Dinsmore, P. K. & Klaenhammer, T. R. ( 1995; ). Bacteriophage resistance in Lactococcus. Mol Biotechnol 4, 297–314.[CrossRef]
    [Google Scholar]
  7. Duckworth, D. H. & Pinkerton, T. C. ( 1988; ). ColIb plasmid genes that inhibit the replication of T5 and T7 bacteriophage. Plasmid 20, 182–193.[CrossRef]
    [Google Scholar]
  8. Duckworth, D. H., Dunn, G. B., Pinkerton, T., Rose, K. & Walia, S. K. ( 1981; ). Colicin activity and abortive infection of T5 bacteriophage in Escherichia coli (ColIb). J Virol 37, 916–921.
    [Google Scholar]
  9. Feldgarden, M., Golden, S., Wilson, H. & Riley, M. A. ( 1995; ). Can phage defence maintain colicin plasmids in Escherichia coli? Microbiology 141, 2977–2984.[CrossRef]
    [Google Scholar]
  10. Garvey, P., Hill, C. & Fitzgerald, G. F. ( 1996; ). The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanism, one which affects phage DNA penetration. Appl Environ Microbiol 62, 676–679.
    [Google Scholar]
  11. Hofer, B., Ruge, M. & Dreiseikelmann, B. ( 1995; ). The superinfection exclusion gene (sieA) of bacteriophage P22: identification and overexpression of the gene and localization of the gene product. J Bacteriol 177, 3080–3086.
    [Google Scholar]
  12. Karlsson, F., Borrebaeck, C. A., Nilsson, N. & Malmborg-Hager, A. C. ( 2003; ). The mechanism of bacterial infection by filamentous phages involves molecular interactions between TolA and phage protein 3 domains. J Bacteriol 185, 2628–2634.[CrossRef]
    [Google Scholar]
  13. Lazdunski, C. J., Bouveret, E., Rigal, A., Journet, L., Lloubes, R. & Benedetti, H. ( 1998; ). Colicin import into Escherichia coli cells. J Bacteriol 180, 4993–5002.
    [Google Scholar]
  14. Lin, Y. H., Liao, C. C., Liang, P. H., Yuan, H. S. & Chak, K. F. ( 2004; ). Involvement of colicin in the limited protection of the colicin producing cells against bacteriophage. Biochem Biophys Res Commun 318, 81–87.[CrossRef]
    [Google Scholar]
  15. Lu, M. J., Stierhof, Y. D. & Henning, U. ( 1993; ). Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4. J Virol 67, 4905–4913.
    [Google Scholar]
  16. Lubkowski, J., Hennecke, F., Pluckthun, A. & Wlodawer, A. ( 1999; ). Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure 7, 711–722.[CrossRef]
    [Google Scholar]
  17. Marvin, D. A. ( 1998; ). Filamentous phage structure, infection and assembly. Curr Opin Struct Biol 8, 150–158.[CrossRef]
    [Google Scholar]
  18. McGrath, S., Fitzgerald, G. F. & van Sinderen, D. ( 2002; ). Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol Microbiol 43, 509–520.[CrossRef]
    [Google Scholar]
  19. Pugsley, A. P. ( 1984; ). The ins and outs of colicins. Part I: production, and translocation across membranes. Microbiol Sci 1, 168–175.
    [Google Scholar]
  20. Rasched, I. & Oberer, E. ( 1986; ). Ff coliphages: structural and functional relationships. Microbiol Rev 50, 401–427.
    [Google Scholar]
  21. Reakes, C. F., Gann, A. A., Rossouw, F. T. & Rowbury, R. J. ( 1987; ). Abortive infection by bacteriophage Me1 of Escherichia coli K12 strains bearing the plasmid ColV, I-K94. J Gen Virol 68, 263–272.[CrossRef]
    [Google Scholar]
  22. Riechmann, L. & Holliger, P. ( 1997; ). The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell 90, 351–360.[CrossRef]
    [Google Scholar]
  23. Riley, M. A. & Gordon, D. M. ( 1992; ). A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages. J Gen Microbiol 138, 1345–1352.[CrossRef]
    [Google Scholar]
  24. Riley, M. A. & Wertz, J. E. ( 2002; ). Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56, 117–137.[CrossRef]
    [Google Scholar]
  25. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY. : Cold Spring Harbor Laboratory.
    [Google Scholar]
  26. Sanders, M. E. & Klaenhammer, T. R. ( 1983; ). Characterization of phage-sensitive mutants from a phage-insensitive strain of Streptococcus lactis: evidence for a plasmid determinant that prevents phage adsorption. Appl Environ Microbiol 46, 1125–1133.
    [Google Scholar]
  27. Schägger, H. & von Jagow, G. ( 1987; ). Tricine–sodium dodecyl sulfate–polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166, 368–379.[CrossRef]
    [Google Scholar]
  28. Stopar, D., Spruijt, R. B., Wolfs, C. J. & Hemminga, M. A. ( 2003; ). Protein–lipid interactions of bacteriophage M13 major coat protein. Biochim Biophys Acta 1611, 5–15.[CrossRef]
    [Google Scholar]
  29. Stopar, D., Spruijt, R. B. & Hemminga, M. A. ( 2006; ). Anchoring mechanisms of membrane-associated M13 major coat protein. Chem Phys Lipids 141, 83–93.[CrossRef]
    [Google Scholar]
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vol. , part 11, pp. 3379 - 3385

Limited protection against M13 bacteriophage exerted by various colicin groups after mitomycin C induction [ PDF] (8 kb)



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