1887

Abstract

The food-borne pathogen has the ability to survive extreme environmental conditions due to an extensive interacting network of stress responses. It is able to grow and survive at relatively high temperatures in comparison with other non-sporulating food-borne pathogens. To investigate the heat-shock response of , whole-genome expression profiles of cells that were grown at 37 °C and exposed to 48 °C were examined using DNA microarrays. Transcription levels were measured over a 40 min period after exposure of the culture to 48 °C and compared with those of unexposed cultures at 37 °C. After 3 min, 25 % of all genes were differentially expressed, while after 40 min only 2 % of all genes showed differential expression, indicative of the transient nature of the heat-shock response. The global transcriptional response was validated by analysing the expression of a set of 13 genes by quantitative PCR. Genes previously identified as part of the class I and class III heat-shock response and the class II stress response showed induction at one or more of the time points investigated. This is believed to be the first study to report that several heat-shock-induced genes are part of the SOS response in . Furthermore, numerous differentially expressed genes that have roles in the cell division machinery or cell wall synthesis were down-regulated. This expression pattern is in line with the observation that heat shock results in cell elongation and prevention of cell division.

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2007-10-01
2024-04-19
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References

  1. Au N., Kuester-Schoeck E., Mandava V., Bothwell L. E., Canny S. P., Chachu K., Colavito S. A., Fuller S. N., Groban E. S. other authors 2005; Genetic composition of the Bacillus subtilis SOS system. J Bacteriol 187:7655–7666
    [Google Scholar]
  2. Autret N., Raynaud C., Dubail I., Berche P., Charbit A. 2003; Identification of the agr locus of Listeria monocytogenes : role in bacterial virulence. Infect Immun 71:4463–4471
    [Google Scholar]
  3. Benson A. K., Haldenwang W. G. 1993; The σ B-dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J Bacteriol 175:1929–1935
    [Google Scholar]
  4. Caldas T., Demont-Caulet N., Ghazi A., Richarme G. 1999; Thermoprotection by glycine betaine and choline. Microbiology 145:2543–2548
    [Google Scholar]
  5. Chakraborty T., Leimeister-Wachter M., Domann E., Hartl M., Goebel W., Nichterlein T., Notermans S. 1992; Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174:568–574
    [Google Scholar]
  6. Chatterjee S. S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T. 2006; Intracellular gene expression profile of Listeria monocytogenes . Infect Immun 74:1323–1338
    [Google Scholar]
  7. Cox M. M., Goodman M. F., Kreuzer K. N., Sherratt D. J., Sandler S. J., Marians K. J. 2000; The importance of repairing stalled replication forks. Nature 404:37–41
    [Google Scholar]
  8. Doorduyn Y., de Jager C. M., van der Zwaluw W. K., Wannet W. J., van der Ende A., Spanjaard L., van Duynhoven Y. T. 2006; First results of the active surveillance of Listeria monocytogenes infections in the Netherlands reveal higher than expected incidence. Euro Surveill 11:E060420–E060424
    [Google Scholar]
  9. Gao H., Wang Y., Liu X., Yan T., Wu L., Alm E., Arkin A., Thompson D. K., Zhou J. 2004; Global transcriptome analysis of the heat shock response of Shewanella oneidensis . J Bacteriol 186:7796–7803
    [Google Scholar]
  10. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P. other authors 2001; Comparative genomics of Listeria species. Science 294:849–852
    [Google Scholar]
  11. Godoy V. G., Jarosz D. F., Walker F. L., Simmons L. A., Walker G. C. 2006; Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression. EMBO J 25:868–879
    [Google Scholar]
  12. Hare J. M., Perkins S. N., Gregg-Jolly L. A. 2006; A constitutively expressed, truncated umuDC operon regulates the recA -dependent DNA damage induction of a gene in Acinetobacter baylyi strain ADP1. Appl Environ Microbiol 72:4036–4043
    [Google Scholar]
  13. Health Protection Agency 2005; The changing epidemiology of listeriosis in England and Wales. Commun Dis Rep CDR Wkly 15:383–4
    [Google Scholar]
  14. Helmann J. D., Wu M. F., Kobel P. A., Gamo F. J., Wilson M., Morshedi M. M., Navre M., Paddon C. 2001; Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol 183:7318–7328
    [Google Scholar]
  15. Henriques A. O., Glaser P., Piggot P. J., Moran C. P. Jr 1998; Control of cell shape and elongation by the rodA gene in Bacillus subtilis . Mol Microbiol 28:235–247
    [Google Scholar]
  16. Holtmann G., Bremer E. 2004; Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters. J Bacteriol 186:1683–1693
    [Google Scholar]
  17. Johansson J., Mandin P., Renzoni A., Chiaruttini C., Springer M., Cossart P. 2002; An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes . Cell 110:551–561
    [Google Scholar]
  18. Kallipolitis B. H., Ingmer H. 2001; Listeria monocytogenes response regulators important for stress tolerance and pathogenesis. FEMS Microbiol Lett 204:111–115
    [Google Scholar]
  19. Karatzas K. A., Valdramidis V. P., Wells-Bennik M. H. 2005; Contingency locus in ctsR of Listeria monocytogenes Scott A: a strategy for occurrence of abundant piezotolerant isolates within clonal populations. Appl Environ Microbiol 71:8390–8396
    [Google Scholar]
  20. Kawai Y., Moriya S., Ogasawara N. 2003; Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis . Mol Microbiol 47:1113–1122
    [Google Scholar]
  21. Kazmierczak M. J., Mithoe S. C., Boor K. J., Wiedmann M. 2003; Listeria monocytogenes σ B regulates stress response and virulence functions. J Bacteriol 185:5722–5734
    [Google Scholar]
  22. Koch J., Stark K. 2006; Significant increase of listeriosis in Germany – epidemiological patterns 2001–2005. Euro Surveill 11:85–88
    [Google Scholar]
  23. Komatsuzawa H., Fujiwara T., Nishi H., Yamada S., Ohara M., McCallum N., Berger-Bachi B., Sugai M. 2004; The gate controlling cell wall synthesis in Staphylococcus aureus . Mol Microbiol 53:1221–1231
    [Google Scholar]
  24. Kruger E., Hecker M. 1998; The first gene of the Bacillus subtilis clpC operon, ctsR , encodes a negative regulator of its own operon and other class III heat shock genes. J Bacteriol 180:6681–6688
    [Google Scholar]
  25. Kruse T., Bork-Jensen J., Gerdes K. 2005; The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55:78–89
    [Google Scholar]
  26. Leimeister-Wachter M., Haffner C., Domann E., Goebel W., Chakraborty T. 1990; Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes . Proc Natl Acad Sci U S A 87:8336–8340
    [Google Scholar]
  27. Leimeister-Wachter M., Domann E., Chakraborty T. 1992; The expression of virulence genes in Listeria monocytogenes is thermoregulated. J Bacteriol 174:947–952
    [Google Scholar]
  28. Lusetti S. L., Cox M. M. 2002; The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71:71–100
    [Google Scholar]
  29. Maul R. W., Sutton M. D. 2005; Roles of the Escherichia coli RecA protein and the global SOS response in effecting DNA polymerase selection in vivo. J Bacteriol 187:7607–7618
    [Google Scholar]
  30. McKenzie G. J., Lee P. L., Lombardo M. J., Hastings P. J., Rosenberg S. M. 2001; SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol Cell 7:571–579
    [Google Scholar]
  31. Michel B. 2005; After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol 3:e255
    [Google Scholar]
  32. Miller C., Thomsen L. E., Gaggero C., Mosseri R., Ingmer H., Cohen S. N. 2004; SOS response induction by β -lactams and bacterial defense against antibiotic lethality. Science 305:1629–1631
    [Google Scholar]
  33. Milohanic E., Glaser P., Coppee J. Y., Frangeul L., Vega Y., Vazquez-Boland J. A., Kunst F., Cossart P., Buchrieser C. 2003; Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 47:1613–1625
    [Google Scholar]
  34. Neuhaus F. C., Baddiley J. 2003; A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67:686–723
    [Google Scholar]
  35. O'Reilly E. K., Kreuzer K. N. 2004; Isolation of SOS constitutive mutants of Escherichia coli . J Bacteriol 186:7149–7160
    [Google Scholar]
  36. Rauch M., Luo Q., Muller-Altrock S., Goebel W. 2005; SigB-dependent in vitro transcription of prfA and some newly identified genes of Listeria monocytogenes whose expression is affected by PrfA in vivo. J Bacteriol 187:800–804
    [Google Scholar]
  37. Rothfield L., Taghbalout A., Shih Y. L. 2005; Spatial control of bacterial division-site placement. Nat Rev Microbiol 3:959–968
    [Google Scholar]
  38. Schmidt K. L., Peterson N. D., Kustusch R. J., Wissel M. C., Graham B., Phillips G. J., Weiss D. S. 2004; A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli . J Bacteriol 186:785–793
    [Google Scholar]
  39. Schulz A., Schumann W. 1996; hrcA , the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J Bacteriol 178:1088–1093
    [Google Scholar]
  40. Sleator R. D., Wouters J., Gahan C. G., Abee T., Hill C. 2001; Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes . Appl Environ Microbiol 67:2692–2698
    [Google Scholar]
  41. Stack H. M., Sleator R. D., Bowers M., Hill C., Gahan C. G. 2005; Role for HtrA in stress induction and virulence potential in Listeria monocytogenes . Appl Environ Microbiol 71:4241–4247
    [Google Scholar]
  42. Stintzi A. 2003; Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J Bacteriol 185:2009–2016
    [Google Scholar]
  43. Wemekamp-Kamphuis H. H., Sleator R. D., Wouters J. A., Hill C., Abee T. 2004; Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. Appl Environ Microbiol 70:2912–2918
    [Google Scholar]
  44. Wilson R. L., Brown L. L., Kirkwood-Watts D., Warren T. K., Lund S. A., King D. S., Jones K. F., Hruby D. E. 2006; Listeria monocytogenes 10403S HtrA is necessary for resistance to cellular stress and virulence. Infect Immun 74:765–768
    [Google Scholar]
  45. Zhou H., Lutkenhaus J. 2005; MinC mutants deficient in MinD- and DicB-mediated cell division inhibition due to loss of interaction with MinD, DicB, or a septal component. J Bacteriol 187:2846–2857
    [Google Scholar]
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