1887

Abstract

It was found that infection of by bacteriophage λ is inhibited in the presence of certain bile salts and carbohydrates when cells are in the ’OFF’ state for production of the phase-variable cell surface protein antigen 43 (Ag43). The inhibition of phage growth was found to be due to a significant impairment in the process of phage adsorption. Expression of the gene encoding Ag43 () from a plasmid or inactivation of the gene (encoding an activator of genes important for defence against oxidative stress) suppressed this inhibition. A mutation, , in the gene encoding the α subunit of RNA polymerase also facilitated phage adsorption in the presence of bile salts and carbohydrates. The mutation promoted efficient production of Ag43 in a genetic background that would otherwise be in the ’OFF’ phase for expression of the gene. Analysis of a reporter gene fusion demonstrated that the promoter for the gene was more active in the mutant than in the otherwise isogenic strain. The combined inhibitory action of bile salts and carbohydrates on phage adsorption and the abolition of this inhibition by production of Ag43 was not restricted to λ, as a similar phenomenon was observed for the coliphages P1 and T4.

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2002-05-01
2024-12-07
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References

  1. Arber W., Enquist L., Hohn B., Murray N. E., Murray K. 1983; Experimental methods for use with lambda. In Lambda II pp 433–466 Edited by Hendrix R. W. Roberts J. W., Stahl F. W., Weisberg R. A. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  2. Bernstein C., Bernstein H., Payne C. M., Beard S. E., Schneider J. 1999; Bile salt activation of stress response promoters in Escherichia coli . Curr Microbiol 39:68–72 [CrossRef]
    [Google Scholar]
  3. Caffrey P., Owen P. 1989; Purification and N-terminal sequence of the α subunit of antigen 43, a unique protein complex associated with the outer membrane of Escherichia coli . J Bacteriol 171:3634–3640
    [Google Scholar]
  4. Casjens S., Hendrix R. 1988; Control mechanisms in dsDNA bacteriophage assembly. In The Bacteriophages pp 15–91 Edited by Calendar R. New York & London: Plenum;
    [Google Scholar]
  5. Danese P. L., Pratt L. A., Dove S. L., Kolter R. 2000; The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol 37:424–432 [CrossRef]
    [Google Scholar]
  6. Diderichsen B. 1980; flu , a metastable gene controlling surface properties of Escherichia coli . J Bacteriol 141:858–867
    [Google Scholar]
  7. Drasar B. S., Barrow P. A. 1985 Intestinal Microbiology: Aspects of Microbiology vol. 10 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  8. Elliott W. H. 1985; Metabolism of bile salts in liver and extrahepatic tissues. In Sterols and Bile Acids pp 303–329 Edited by Danielsson H. Sjovall J. New York: Elsevier;
    [Google Scholar]
  9. Gabig M., Obuchowski M., Ciesielska A., Latała B., Thomas M. S., Wȩgrzyn A., Wȩgrzyn G. 1998; The Escherichia coli RNA polymerase α subunit and transcriptional activation by bacteriophage λ CII protein. Acta Biochim Pol 45:271–280
    [Google Scholar]
  10. Giffard P. M., Booth I. R. 1988; The rpoA341 allele of Escherichia coli specifically impairs the transcription of group of positively regulated operons. Mol Gen Genet 214:148–152 [CrossRef]
    [Google Scholar]
  11. Giladi H., Koby S., Gottesman M. E., Oppenheim A. B. 1992; Supercoiling, integration host factor, and a dual promoter system participate in the control of the bacteriophage λ pL promoter. J Mol Biol 224:937–948 [CrossRef]
    [Google Scholar]
  12. Goldberg A. R., Howe M. 1969; New mutations in the S cistron of bacteriophage lambda affecting host cell lysis. Virology 38:200–202 [CrossRef]
    [Google Scholar]
  13. Gonzalez-Flecha B., Demple B. 1997; Transcriptional regulation of the Escherichia coli oxyR gene as a function of cell growth. J Bacteriol 179:6181–6186
    [Google Scholar]
  14. Haagmans W., van der Woude M. 2000; Phase variation of Ag43 in Escherichia coli : Dam-dependent methylation abrogates OxyR binding and OxyR-mediated repression of transcription. Mol Microbiol 35:877–887 [CrossRef]
    [Google Scholar]
  15. Hancock R. E. W. 1997; The bacterial outer membrane as a drug barrier. Trends Microbiol 5:37–42 [CrossRef]
    [Google Scholar]
  16. Hasman H., Chakraborty T., Klemm P. 1999; Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181:4834–4841
    [Google Scholar]
  17. Hasman H., Schembri M. A., Klemm P. 2000; Antigen 43 and type 1 fimbriae determine colony morphology of Escherichia coli K-12. J Bacteriol 182:1089–1095 [CrossRef]
    [Google Scholar]
  18. Henderson I. R., Owen P. 1999; The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J Bacteriol 181:2132–2141
    [Google Scholar]
  19. Henderson I. R., Meehan M., Owen P. 1997; A novel regulatory mechanism for a novel phase-variable outer membrane protein of Escherichia coli . In Mechanisms in the Pathogenesis of Enteric Diseases: Advances in Experimental Medicine and Biology vol. 412 Edited by Paul P. S. Francis D. H., Benfield D. A. New York: Plenum;
    [Google Scholar]
  20. Jensen K. F. 1993; The Escherichia coli ‘wild types’ W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol 175:3401–3407
    [Google Scholar]
  21. Kȩdzierska S., Staniszewska M., Potrykus J., Wȩgrzyn G. 1999; The effect of some antibiotic-resistance-conferring plasmids on the removal of the heat-aggregated proteins from Escherichia coli cells. FEMS Microbiol Lett 176:279–284 [CrossRef]
    [Google Scholar]
  22. Kjaergaard K., Schembri M. A., Ramos C., Molin S., Klemm P. 2000a; Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol 2:695–702 [CrossRef]
    [Google Scholar]
  23. Kjaergaard K., Schembri M. A., Hasman H., Klemm P. 2000b; Antigen 43 from Escherichia coli induces inter- and intraspecies cell aggregation and changes in colony morphology of Pseudomonas fluorescens . J Bacteriol 182:4789–4796 [CrossRef]
    [Google Scholar]
  24. Kucharczyk K., Laskowska E., Taylor A. 1991; Response of Escherichia coli cell membranes to induction of λ cI857 prophage by heat shock. Mol Microbiol 5:2935–2945 [CrossRef]
    [Google Scholar]
  25. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  26. Obuchowski M., Giladi H., Koby S., Szalewska-Pałasz A., Oppenheim A. B., Thomas M. S., Wȩgrzyn A., Wȩgrzyn G. 1997; Impaired lysogenization of the Escherichia coli rpoA341 mutant by bacteriophage λ is due to the inability of CII to act as a transcriptional activator. Mol Gen Genet 254:304–311 [CrossRef]
    [Google Scholar]
  27. Owen P. 1992; The Gram-negative outer membrane: structure, biochemistry and vaccine potential. Biochem Soc Trans 20:1–6
    [Google Scholar]
  28. Owen P., Caffrey P., Josefsson L. G. 1987; Identification and partial characterization of a novel bipartite protein antigen associated with the outer membrane of Escherichia coli . J Bacteriol 169:3770–3777
    [Google Scholar]
  29. Pope L. M., Reed K. E., Payne S. M. 1995; Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect Immun 63:3642–3648
    [Google Scholar]
  30. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Silhavy S. J., Berman M. L., Enquist L. W. 1984 Experiments with Gene Fusions. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  32. Szalewska A., Taylor K., Wȩgrzyn G. 1994; Neither absence nor excess of λ O initiator-digesting ClpXP protease affects λ plasmid or phage replication in Escherichia coli . Mol Microbiol 13:469–474 [CrossRef]
    [Google Scholar]
  33. Szalewska-Pałasz A., Obuchowski M., Pawłowski R., Bielawski K., Thomas M. S., Wȩgrzyn A., Wȩgrzyn G. 1996; Drastically decreased transcription from CII-activated promoters is responsible for impaired lysogenization of the Escherichia coli rpoA341 mutant by bacteriophage λ. FEMS Microbiol Lett 144:21–27
    [Google Scholar]
  34. Thomas M. S., Glass R. E. 1991; Escherichia coli rpoA mutation which impairs transcription of positively regulated systems. Mol Microbiol 5:2719–2725 [CrossRef]
    [Google Scholar]
  35. Warne S. R., Varley J. M., Boulnois G. J., Norton M. G. 1990; Identification and characterization of a gene that controls colony morphology and auto-aggregation in Escherichia coli K12. J Gen Microbiol 136:455–462 [CrossRef]
    [Google Scholar]
  36. Wȩgrzyn G., Glass R. E., Thomas M. S. 1992; Involvement of the Escherichia coli RNA polymerase α subunit in transcriptional activation by the bacteriophage lambda CI and CII proteins. Gene 122:1–7 [CrossRef]
    [Google Scholar]
  37. Williams-Smith H. 1965; Observations on the flora of the alimentary tract of animals and factors its composition. J Pathol Bacteriol 89:95–122 [CrossRef]
    [Google Scholar]
  38. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strain: nucleotide sequence of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
    [Google Scholar]
  39. Zheng M., Doan B., Schneider T. D., Storz G. 1999; OxyR and SoxRS regulation of fur . J Bacteriol 181:4639–4643
    [Google Scholar]
  40. Zilberstein D., Padan E., Schuldiner S. 1980; A single locus in Escherichia coli governs growth in alkaline pH and on carbon sources whose transport is sodium-dependent. FEBS Lett 168:327–330
    [Google Scholar]
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