Skip to main content
SpringerLink
Log in

Lysogenic infection of a Shiga toxin 2-converting bacteriophage changes host gene expression, enhances host acid resistance and motility

  • Cell Molecular Biology
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Shiga toxin 2 (Stx2)-converting bacteriophages ca n infect and lysogenized other bacteria in vivo and in vitro, and thus contribute to the genotypic heterogeneity of infected host. However, the global transcription patterns accompanying the lysogenic infection of Escherichia coli coli host have not been clearly resolved. In this study, we compared the gene expression profiles of Stx2 phage ΦMin27(Δstx::cat) converted and naïve E. coli MG1655 hosts using microarray analyses. It was identified that conversion by ΦMin27(Δstx::cat) had a direct effect on the global expression of bacterial host genes as 166 genes were found to be differentially expressed (104 up-regulated and 62 down-regulated). These genes were predominantly responsible for bacterial central metabolism, transport and transcription. It was shown that in addition to the down-regulation of genes involved in synthesis of Thi an d protein transporters, expression of genes associated with bacterial energy production (e.g., fadABDEHIJL, aceK and acnA) were also suppressed. Conversely, a significantly larger number of genes were up-regulated, including transport genes, flagellar synthesis genes (fliDESTZ) and acid resistant genes (e.g., gadEW, hdeABD and adiY). Our study also discovered conversion of ΦMin27(Δstx::cat) could change host physiological character. The converted cells had increased acid tolerance at low pH and promoted swimming motility on semisolid agar surface compared to the uninfected bacterial host.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Gyles C.L. 2007. Shiga toxin-producing Escherichia coli: An overview. J. Anim. Sci. 85, 45–62.

    Article  Google Scholar 

  2. O’Brien A.D., Newland J.W., Miller S.F., Holmes R.K., Smith H.W., Formal S.B. 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science. 226, 694–696.

    Article  PubMed  Google Scholar 

  3. Gamage S.D., Strasser J.E., Chalk C.L., Weiss A.A. 2003. Nonpathogenic Escherichia coli can contribute to the production of Shiga toxin. Infect. Immun. 71, 3107–3115.

    Article  PubMed  CAS  Google Scholar 

  4. Cornick N.A., Helgerson A.F., Mai V., Ritchie J.M., Acheson D.W. 2006. In vivo transduction of an Stx-encoding phage in ruminants. Appl. Environ. Microbiol. 72, 5086–5088.

    Article  PubMed  CAS  Google Scholar 

  5. Heuvelink A.E., VandeKar N.C., Meis J.F., Monnens L.A., Melchers W.J. 1995. Characterization of verocytotoxin-producing Escherichia coli O157 isolates from patients with haemolytic uraemic syndrome in Western Europe. Epidemiol. Infect. 115, 1–14.

    Article  PubMed  CAS  Google Scholar 

  6. Thomas A., Cheasty T., Chart H., Rowe B. 1994. Isolation of Vero cytotoxin-producing Escherichia coli sero-types O9ab:H- and O101: H- carrying VT2 variant gene sequences from a patient with haemolytic uraemic syndrome. Eur. J. Clin. Microbiol. Infect. Dis. 13, 1074–1076.

    Article  PubMed  CAS  Google Scholar 

  7. Herold S., Karch H., Schmidt H. 2004. Shiga toxin-encoding bacteriophages: Genomes in motion. Int. J. Med. Microbiol. 294, 115–121.

    Article  PubMed  CAS  Google Scholar 

  8. Schmidt H. 2001. Shiga-toxin-converting bacteriophages. Res. Microbiol. 152, 687–695.

    Article  PubMed  CAS  Google Scholar 

  9. Allison, H.E. 2007. Stx-phages: Drivers and mediators of the evolution of STEC and STEC-like pathogens. Future. Microbiol. 2, 165–174.

    Article  PubMed  CAS  Google Scholar 

  10. James C.E., Stanley K.N., Allison H.E., Flint H.J., Stewart C.S., Sharp R.J., Saunders J.R., McCarthy A.J. 2001. Lytic and lysogenic infection of diverse Escherichia coli and Shigella strains with a verocytotoxigenic bacteriophage. Appl. Environ. Microbiol. 67, 4335–4337.

    Article  PubMed  CAS  Google Scholar 

  11. Muniesa M., Blanco J.E., Simãn M.D., Serra-Moreno R., Blanch A.R., Jofre J. 2004. Diversity of stx2 converting bacteriophages induced from Shiga-toxin-producing Escherichia coli strains isolated from cattle. Microbiology. 150, 2959–2971.

    Article  PubMed  CAS  Google Scholar 

  12. Mühldorfer I., Hacker J., Keusch G.T., Acheson D.W., Tschäpe H., Kane A.V., Ritter A., Ölschläger T., Dono-hue-rolfe A. 1996. Regulation of the Shiga-like toxin II operon in Escherichia coli. Infect. Immun. 64, 495–502.

    PubMed  Google Scholar 

  13. Wagner P.L., Acheson D.W., Waldor M.K. 2001. Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichia coli. Infect. Immun. 69, 1934–1937.

    CAS  Google Scholar 

  14. Letellier L., Plancon L., Bonhivers M., Boulanger P. 1999. Phage DNA transport across membranes. Res. Microbiol. 150, 499–505.

    Article  PubMed  CAS  Google Scholar 

  15. Nash H.A. 1981. Integration and excision of bacteriophage lambda: The mechanism of conservation site specific recombination. Annu. Rev. Genet. 15, 143–167.

    Article  PubMed  CAS  Google Scholar 

  16. Harrington C.A., Rosenow C., Retief J. 2000. Monitoring gene expression using DNA microarrays. Curr. Opin. Microbiol. 3, 285–291.

    Article  PubMed  CAS  Google Scholar 

  17. Osterhout R.E., Figueroa I.A., Keasling J.D., Arkin A.P. 2007. Global analysis of host response to induction of a latent bacteriophage. BMC Microbiol. 7, 82–93.

    Article  PubMed  CAS  Google Scholar 

  18. Herold S., Siebert J., Huber A., Schmidt H. 2005. Global expression of prophage genes in Escherichia coli O157:H7 strain EDL933 in response to norfloxacin. Antimicrob. Agents. Chemother. 49, 931–944.

    Article  PubMed  CAS  Google Scholar 

  19. Karlsson F., Malmborg-Hager A.C., Albrekt A.S., Borrebaeck C.A. 2005. Genome-wide comparison of phage M13-infected vs. uninfected Escherichia coli. Can. J. Microbiol. 51, 29–35.

    CAS  Google Scholar 

  20. Liangke Su., Yaxian Y., Chengping L. 2008. Construction of a stx2 deletion mutant of Shiga toxin 2 phage ΦMin27 and its infectious properties. Acta Microbiol. Sinica. 48, 1227–1233.

    Google Scholar 

  21. Blattner F.R., Plunkett G.III., Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science. 277, 1453–1474.

    Article  PubMed  CAS  Google Scholar 

  22. Schmidt H., Bielaszewska M., Karch H. 1999. Transduction of enteric Escherichia coli isolates with a derivative of Shiga toxin 2-encoding bacteriophage Φ3538 isolated from Escherichia coli O157:H7. Appl. Environ. Microbiol. 65, 3855–3861.

    PubMed  CAS  Google Scholar 

  23. Livak K.J., Schmittgen T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 —Δ0394;Ct method. Methods. 25, 402–408.

    Article  PubMed  CAS  Google Scholar 

  24. Castanie-Cornet M.P., Penfound T.A., Smith D., Elliott J.F., Foster J.W. 1999. Control of acid resistance in Escherichia coli. J. Bacteriol. 181, 3525–3535.

    CAS  Google Scholar 

  25. Gãmez-Gãmez J.M., Manfredi C., Alonso J.C., Blázquez J. 2007. A novel role for RecA under non-stress: promotion of swarming motility in Escherichia coli K-12. BMC. Biol. 5, 1–15.

    Article  CAS  Google Scholar 

  26. Zorzano M.P., Hochberg D., Cuevas M.T., Gãmez-Gãmez J.M. 2005. Reaction-diffusion model for pattern formation in E. coli swarming colonies with slime. Phys. Rev. E. Stat. Nonlin. Soft. Matter. Phys. 71, 031908.

    PubMed  Google Scholar 

  27. Boucher D.J., Adler B., Boyce J.D. 2005. The Pasteurella multocida nrfE gene is upregulated during infection and is essential for nitrite reduction but not for virulence. J. Bacteriol. 187, 2278–2285.

    Article  PubMed  CAS  Google Scholar 

  28. Mao H., Cremer P.S., Manson M.D. 2003. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc. Natl. Acad. Sci. USA. 100, 5449–5454.

    Article  PubMed  CAS  Google Scholar 

  29. Tucker D.L., Tucker N., Conway T. 2002. Gene expression profiling of the pH response in Escherichia coli. J. Bacterial. 184, 6551–6558.

    CAS  Google Scholar 

  30. Hommais F., Krin E., Coppee J.Y., Lacroix C., Yeramian E., Danchin A., Bertin P. 2004. GadE (YhiE): A novel activator involved in the response to acid environment in Escherichia coli. Microbiology. 150, 61–72.

    CAS  Google Scholar 

  31. Kieboom J., Abee T. 2006. Arginine-dependent acid resistance in Salmonella enteric serovar Typhimurium. J. Bacteriol. 188, 5650–5653.

    Article  PubMed  CAS  Google Scholar 

  32. Horn P.B.V., Backstrom A., Stewart V., Begley T.P. 1993. Structural genes for thiamine biosynthetic enzymes (thiCEFGH) in Escherichia coli K-12. J. Bacteriol. 175, 982–992.

    Google Scholar 

  33. Higgins C.F. 2001. ABC transporters: Physiology, structure and mechanism—an overview. Res. Microbiol. 152, 205–210.

    Article  PubMed  CAS  Google Scholar 

  34. Cho B.K., Knight E.M., Palsson B. 2006. Transcriptional regulation of the fad regulon genes of Escherichia coli by ArcA. Microbiology. 152, 2207–2219.

    Article  PubMed  CAS  Google Scholar 

  35. Reed L.J. 1953. Metabolic functions of thiamine and lipoic acid. Physiol Rev. 33, 544–559.

    PubMed  CAS  Google Scholar 

  36. Friedman D.A., Olson E.R., Georgopoulos C.G., Tilly K., Herskowitz I., Banuett F. 1984. Interactions of bacteriophage and host macromolecules in the growth of bacteriophage 7n. Microbiol. Rev. 48, 299–325.

    PubMed  CAS  Google Scholar 

  37. Miller H.I., Nash N.A. 1981. Direct role of the himA gene product in phage 7n integration. Nature. 290, 523–526.

    Article  PubMed  CAS  Google Scholar 

  38. Willenbrock H., Petersen A., Sekse C., Kiil K., Wasteson Y., Ussery D.W. 2006. Design of a seven-genome Escherichia coli microarray for comparative genomic profiling. J. Bacteriol. 188, 7713–7721.

    Article  PubMed  CAS  Google Scholar 

  39. Wolfe A.J., Berg H.C. 1989. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. USA. 86, 6973–6977.

    Article  PubMed  CAS  Google Scholar 

  40. Garrity L.F., Ordal G.W. 1995. Chemotaxis in Bacillus subtilis: How bacteria monitor environmental signals. Pharmacol. Ther. 68, 87–104.

    Article  PubMed  CAS  Google Scholar 

  41. Parkinson J.S., Parker S.R., Talbert P.B., Houts S.E. 1983. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J. Bacteriol. 155, 265–274.

    CAS  Google Scholar 

  42. Blair D.F. 1995. How bacteria sense and swim. Annu. Rev. Microbiol. 49, 489–522.

    Article  PubMed  CAS  Google Scholar 

  43. Tucker D.L., Tucker N., Conway T. 2002. Gene expression profiling of the pH response in Escherichia coli. J. Bacteriol. 184, 6551–6558.

    CAS  Google Scholar 

  44. Molina P.M., Parma A.E., Sanz M.E. 2003. Survival in acidic and alcoholic medium of Shiga toxin-producing Escherichia coli O157:H7 and non-O157:H7 isolated in Argentina. BMC Microbiol. 3, 1–6.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Shanghai Key Laboratory of Veterinary Biotechnology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240, China

    L. K. Su, C. P. Lu, Y. Wang, D. M. Cao, J. H. Sun & Y. X. Yan

  2. Key Laboratory of Animal Disease Diagnosis and Immunology of Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    C. P. Lu

Authors
  1. L. K. Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. P. Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. M. Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. H. Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Y. X. Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. X. Yan.

Additional information

The article was submitted by the authors in English

Rights and permissions

Reprints and permissions

About this article

Cite this article

Su, L.K., Lu, C.P., Wang, Y. et al. Lysogenic infection of a Shiga toxin 2-converting bacteriophage changes host gene expression, enhances host acid resistance and motility. Mol Biol 44, 54–66 (2010). https://doi.org/10.1134/S0026893310010085

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893310010085

Key words

Search

Navigation