1887

Abstract

The expression of bacterial cold-shock proteins (CSPs) is highly induced in response to cold shock, and some CSPs are essential for cells to resume growth at low temperature. encodes five CSPs (named CspA to CspE) with significant amino acid homology to CspA of . In contrast to , the insertional knock-out of a single gene () strongly affected growth of independent of temperature. In the case of three of the genes (, , ) more than one specific transcript could be detected. The net amount of , and transcripts increased strongly after cold shock, while no such effect could be observed for and . The exposure to other stress conditions, including translation inhibitors, heat shock, osmotic stress and nutrient deprivation in the stationary phase, indicated that the genes are also responsive to these conditions. The coding regions of all of the cold-shock genes are preceded by a long non-translated upstream region (5′-UTR). In the case of the gene, a deletion of parts of this region led to a significant reduction of translation of the resulting truncated transcript, indicating a role of the 5′-UTR in translational control. The cold-shock stimulon was investigated by 2D-PAGE and mass spectrometric characterization, leading to the identification of additional cold-inducible proteins (CIPs). Interestingly, two cold-shock genes ( and ) were found to be under the negative control of the BvgAS system, the main transcriptional regulator of virulence genes. Moreover, a negative effect of slight overexpression of CspB, but not of the other CSPs, on the transcription of the adenylate cyclase toxin CyaA of was observed, suggesting cross-talk between the CSP-mediated stress response stimulon and the virulence regulon.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27785-0
2005-06-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/6/mic1511895.html?itemId=/content/journal/micro/10.1099/mic.0.27785-0&mimeType=html&fmt=ahah

References

  1. Arico, B., Gross, R., Smida, J. & Rappuoli, R. ( 1987; ). Evolutionary relationships in the genus Bordetella. Mol Microbiol 1, 301–308.[CrossRef]
    [Google Scholar]
  2. Bae, W., Jones, P. G. & Inouye, M. ( 1997; ). CspA, the major cold shock protein of Escherichia coli, negatively regulates its own gene expression. J Bacteriol 179, 7081–7088.
    [Google Scholar]
  3. Bae, W., Xia, B., Inouye, M. & Severinov, K. ( 2000; ). Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc Natl Acad Sci U S A 97, 7784–7789.[CrossRef]
    [Google Scholar]
  4. Banemann, A., Deppisch, H. & Gross, R. ( 1997; ). The lipopolysaccharide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides. Infect Immun 66, 5607–5612.
    [Google Scholar]
  5. Bock, A. & Gross, R. ( 2001; ). The BvgAS two-component system of Bordetella spp. a versatile modulator of virulence gene expression. Int J Med Microbiol 291, 119–130.[CrossRef]
    [Google Scholar]
  6. Brandi, A., Pietroni, P., Gualerzi, C. O. & Pon, C. L. ( 1996; ). Post-transcriptional regulation of CspA expression in Escherichia coli. Mol Microbiol 19, 231–240.[CrossRef]
    [Google Scholar]
  7. Bycroft, M., Hubbard, T. J., Proctor, M., Freund, S. M. & Murzin, A. G. ( 1997; ). The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88, 235–242.[CrossRef]
    [Google Scholar]
  8. Carbonetti, N. H., Fuchs, T. M., Patamawenu, A. A., Irish, T. J., Deppisch, H. & Gross, R. ( 1994; ). Effect of mutations causing overexpression of RNA polymerase alpha subunit on regulation of virulence factors in Bordetella pertussis. J Bacteriol 176, 7267–7273.
    [Google Scholar]
  9. Cormack, B. P., Valdivia, R. H. & Falkow, S. ( 1996; ). FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33–38.[CrossRef]
    [Google Scholar]
  10. Cotter, P. A. & DiRita, V. J. ( 2000; ). Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54, 519–565.[CrossRef]
    [Google Scholar]
  11. Derzelle, S., Hallet, B., Francis, K. P., Ferain, T., Delcour, J. & Hols, P. ( 2000; ). Changes in cspL, cspP, and cspC mRNA abundance as a function of cold shock and growth phase in Lactobacillus plantarum. J Bacteriol 182, 5105–5113.[CrossRef]
    [Google Scholar]
  12. Devereux, J., Haeberli, P. & Smithies, O. ( 1984; ). A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12, 387–395.[CrossRef]
    [Google Scholar]
  13. Fang, L., Jiang, W., Bae, W. & Inouye, M. ( 1997; ). Promoter-independent cold-shock induction of cspA and its derepression at 37 °C by mRNA stabilization. Mol Microbiol 23, 355–364.[CrossRef]
    [Google Scholar]
  14. Ferianc, P., Farewell, A. & Nyström, T. ( 1998; ). The cadmium-stress stimulon of Escherichia coli K-12. Microbiology 144, 1045–1050.[CrossRef]
    [Google Scholar]
  15. Friedman, A. M., Long, S. R., Brown, S. E., Buikema, W. J. & Ausubel, F. M. ( 1982; ). Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene 18, 289–296.[CrossRef]
    [Google Scholar]
  16. Fuchs, T. M., Deppisch, H., Scarlato, V. & Gross, R. ( 1996; ). A new gene locus of Bordetella pertussis defines a novel family of prokaryotic transcriptional accessory proteins. J Bacteriol 178, 4445–4452.
    [Google Scholar]
  17. Gerlach, G., von Wintzingerode, F., Middendorf, B. & Gross, R. ( 2001; ). Evolutionary trends in the genus Bordetella. Microbes Infect 3, 61–72.[CrossRef]
    [Google Scholar]
  18. Goodnow, R. A. ( 1980; ). Biology of Bordetella bronchiseptica. Microbiol Rev 44, 722–738.
    [Google Scholar]
  19. Goyard, S. & Ullmann, A. ( 1991; ). Analysis of Bordetella pertussis cya operon regulation by use of cya-lac fusions. FEMS Microbiol Lett 61, 251–256.
    [Google Scholar]
  20. Graumann, P. L. & Marahiel, M. A. ( 1998; ). A superfamily of proteins that contain the cold-shock domain. Trends Biochem Sci 23, 286–290.[CrossRef]
    [Google Scholar]
  21. Graumann, P., Schröder, K., Schmid, R. & Marahiel, M. A. ( 1996; ). Cold shock stress-induced proteins in Bacillus subtilis. J Bacteriol 178, 4611–4619.
    [Google Scholar]
  22. Graumann, P., Wendrich, T. M., Weber, M. H., Schröder, K. & Marahiel, M. A. ( 1997; ). A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol Microbiol 25, 741–756.[CrossRef]
    [Google Scholar]
  23. Gross, R. & Rappuoli, R. ( 1988; ). Positive regulation of pertussis toxin expression. Proc Natl Acad Sci U S A 85, 3913–3917.[CrossRef]
    [Google Scholar]
  24. Gross, R. & Rappuoli, R. ( 1989; ). Pertussis toxin promoter sequences involved in modulation. J Bacteriol 171, 4026–4030.
    [Google Scholar]
  25. Gualerzi, C. O., Giuliodori, A. M. & Pon, C. L. ( 2003; ). Transcriptional and post-transcriptional control of cold-shock genes. J Mol Biol 331, 527–539.[CrossRef]
    [Google Scholar]
  26. Jiang, W., Fang, L. & Inouye, M. ( 1996; ). The role of the 5′-end untranslated region of the mRNA for CspA, the major cold-shock protein of Escherichia coli, in cold-shock adaptation. J Bacteriol 178, 4919–4925.
    [Google Scholar]
  27. Jiang, W., Hou, Y. & Inouye, M. ( 1997; ). CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272, 196–202.[CrossRef]
    [Google Scholar]
  28. Jones, P. G. & Inouye, M. ( 1994; ). The cold-shock response – a hot topic. Mol Microbiol 11, 811–818.[CrossRef]
    [Google Scholar]
  29. Jones, P. G., VanBogelen, R. A. & Neidhardt, F. C. ( 1987; ). Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169, 2092–2095.
    [Google Scholar]
  30. Kimmel, B., Bosserhoff, A., Frank, R., Gross, R., Goebel, W. & Beier, D. ( 2000; ). Identification of immunodominant antigens from Helicobacter pylori and evaluation of their reactivities with sera from patients with different gastroduodenal pathologies. Infect Immun 68, 915–920.[CrossRef]
    [Google Scholar]
  31. Knapp, S. & Mekalanos, J. J. ( 1988; ). Two trans-acting regulatory genes (vir and mod) control antigenic modulation in Bordetella pertussis. J Bacteriol 170, 5059–5066.
    [Google Scholar]
  32. König, J., Bock, A., Perraud, A.-L., Fuchs, T. M., Beier, D. & Gross, R. ( 2002; ). Regulatory factors of Bordetella pertussis affecting virulence gene expression. J Mol Microbiol Biotechnol 4, 197–203.
    [Google Scholar]
  33. Mayr, B., Kaplan, T., Lechner, S. & Scherer, S. ( 1996; ). Identification and purification of a family of dimeric major cold shock protein homologs from the psychrotrophic Bacillus cereus WSBC 10201. J Bacteriol 178, 2916–2925.
    [Google Scholar]
  34. Monack, D. M., Arico, B., Rappuoli, R. & Falkow, S. ( 1989; ). Phase variants of Bordetella bronchiseptica arise by spontaneous deletions in the vir locus. Mol Microbiol 3, 1719–1728.[CrossRef]
    [Google Scholar]
  35. Morales, V. M., Backman, A. & Bagdasarian, M. ( 1991; ). A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97, 39–47.[CrossRef]
    [Google Scholar]
  36. Nyström, T. & Neidhardt, F. C. ( 1996; ). Effects of overproducing the universal stress protein, UspA, in Escherichia coli K-12. J Bacteriol 178, 927–930.
    [Google Scholar]
  37. O'Farrell, P. H. ( 1975; ). High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250, 4007–4021.
    [Google Scholar]
  38. Parkhill, J., Sebaihia, M., Preston, A. & 50 other authors ( 2003; ). Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35, 32–40.[CrossRef]
    [Google Scholar]
  39. Phan-Thanh, L. & Gormon, T. ( 1997; ). Stress proteins in Listeria monocytogenes. Electrophoresis 18, 1464–1471.[CrossRef]
    [Google Scholar]
  40. Porter, J. F., Parton, R. & Wardlaw, A. C. ( 1991; ). Growth and survival of Bordetella bronchiseptica in natural waters and in buffered saline without added nutrients. Appl Environ Microbiol 57, 1202–1206.
    [Google Scholar]
  41. Sambrook, J. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Sanger, F., Nicklen, S. & Coulson, A. R. ( 1977; ). DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74, 5463–5467.[CrossRef]
    [Google Scholar]
  43. Schneider, B. ( 2001; ). Intracellular survival mechanisms of Bordetella species in professional phagocytes. Dissertation, University of Würzburg.
  44. Schneider, B., Gross, R. & Haas, A. ( 2000; ). Phagosome acidification has opposite effects on intracellular survival of Bordetella pertussis and B. bronchiseptica. Infect Immun 68, 7039–7048.[CrossRef]
    [Google Scholar]
  45. Schneider, B., Stübs, D. & Gross, R. ( 2002; ). Identification and genomic organization of gene loci negatively controlled by the virulence regulatory BvgAS two-component system in Bordetella bronchiseptica. Mol Genet Genomics 267, 526–535.[CrossRef]
    [Google Scholar]
  46. Simon, R., Priefer, U. & Pühler, A. ( 1983; ). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1, 784–791.[CrossRef]
    [Google Scholar]
  47. Stainer, D. W. & Scholte, M. J. ( 1970; ). A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol 63, 211–220.[CrossRef]
    [Google Scholar]
  48. Stenson, T. H. & Peppler, M. S. ( 1995; ). Identification of two bvg-repressed surface proteins of Bordetella pertussis. Infect Immun 63, 3780–3789.
    [Google Scholar]
  49. Stibitz, S. & Yang, M. S. ( 1991; ). Subcellular localization and immunological detection of proteins encoded by the vir locus of Bordetella pertussis. J Bacteriol 173, 4288–4296.
    [Google Scholar]
  50. VanBogelen, R. A. & Neidhardt, F. C. ( 1990; ). Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A 87, 5589–5593.[CrossRef]
    [Google Scholar]
  51. von Wintzingerode, F., Schattke, A., Siddiqui, R. A., Rosick, U., Gobel, U. B. & Gross, R. ( 2001; ). Bordetella petrii sp. nov., isolated from an anaerobic bioreactor, and emended description of the genus Bordetella. Int J Syst Evol Microbiol 51, 1257–1265.
    [Google Scholar]
  52. Wang, N., Yamanaka, K. & Inouye, M. ( 1999; ). CspI, the ninth member of the CspA family of Escherichia coli, is induced upon cold shock. J Bacteriol 181, 1603–1609.
    [Google Scholar]
  53. Weiss, A. A. ( 1992; ). The genus Bordetella. In The Prokaryotes, 2nd edn, pp. 2530–2543. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer. New York: Springer.
  54. Weiss, A. A. & Falkow, S. ( 1984; ). Genetic analysis of phase change in Bordetella pertussis. Infect Immun 43, 263–269.
    [Google Scholar]
  55. Wouters, J. A., Sanders, J. W., Kok, J., de Vos, W. M., Kuipers, O. P. & Abee, T. ( 1998; ). Clustered organization and transcriptional analysis of a family of five csp genes of Lactococcus lactis MG1363. Microbiology 144, 2885–2893.[CrossRef]
    [Google Scholar]
  56. Xia, B., Ke, H. & Inouye, M. ( 2001; ). Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol Microbiol 40, 179–188.[CrossRef]
    [Google Scholar]
  57. Yamanaka, K. & Inouye, M. ( 1997; ). Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli. J Bacteriol 179, 5126–5130.
    [Google Scholar]
  58. Yamanaka, K., Fang, L. & Inouye, M. ( 1998; ). The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol Microbiol 27, 247–255.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27785-0
Loading
/content/journal/micro/10.1099/mic.0.27785-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error