1887

Abstract

The expression of the W23 genes specifying the biosynthesis of the major wall teichoic acid, the poly(ribitol phosphate), was studied under phosphate limitation using reporter fusions. Three different regulation patterns can be deduced from these -galactosidase activity data: (i) and gene expression is downregulated under phosphate starvation; (ii) and, to a minor extent, expression after an initial decrease unexpectedly increases; and (iii) is not influenced by phosphate concentration. To dissect the regulatory pattern, its two promoters were analysed under phosphate limitation: The P-ext promoter is repressed under phosphate starvation by the PhoPR two-component system, whereas, under the same conditions, the P-int promoter is upregulated by the action of an extracytoplasmic function (ECF) factor, . In contrast to strain 168, is activated in strain W23 in phosphate-depleted conditions, a phenomenon indirectly dependent on PhoPR, the two-component regulatory system responsible for the adaptation to phosphate starvation. These results provide further evidence for the role of in cell-wall stress response, and suggest that impairment of cell-wall structure is the signal activating this ECF factor.

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2005-09-01
2019-10-17
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References

  1. Antoniewski, C., Savelli, B. & Stragier, P. ( 1990; ). The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally reponsive genes. J Bacteriol 172, 86–93.
    [Google Scholar]
  2. Cao, M. & Helmann, J. D. ( 2002; ). Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function σ factors. J Bacteriol 184, 6123–6129.[CrossRef]
    [Google Scholar]
  3. Cao, M., Wang, T., Ye, R. & Helmann, J. D. ( 2002a; ). Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis σ W and σ M regulons. Mol Microbiol 45, 1267–1276.[CrossRef]
    [Google Scholar]
  4. Cao, M., Kobel, P. A., Morshedi, M. M., Winston Wu, M. F., Paddon, C. & Helmann, J. D. ( 2002b; ). Defining the Bacillus subtilis σ W regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (roma), and transcriptional profiling approaches. J Mol Biol 316, 443–457.[CrossRef]
    [Google Scholar]
  5. Cheah, S. C., Hussey, H., Hancock, I. & Baddiley, J. ( 1982; ). Control of synthesis of wall teichoic acid during balanced growth of Bacillus subtilis W23. J Gen Microbiol 128, 593–599.
    [Google Scholar]
  6. Ellwood, D. C. & Tempest, D. W. ( 1972; ). Effects of environment on bacterial wall content and composition. Adv Microb Physiol 7, 83–117.
    [Google Scholar]
  7. Glaser, P., Kunst, F., Arnaud, M. & 14 other authors ( 1993; ). Bacillus subtilis genome project: cloning and sequencing of the 97 kb region from 325° to 333°. Mol Microbiol 10, 371–384.[CrossRef]
    [Google Scholar]
  8. Grant, W. D. ( 1979; ). Cell wall teichoic acids as a reserve phosphate source in Bacillus subtilis. J Bacteriol 137, 35–43.
    [Google Scholar]
  9. Guérot-Fleury, A.-M., Shazand, K., Frandsen, N. & Stragier, P. ( 1995; ). Antibiotic resistance cassettes for Bacillus subtilis. Gene 167, 335–336.[CrossRef]
    [Google Scholar]
  10. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 16, 557–580.
    [Google Scholar]
  11. Hanahan, D., Jessee, J. & Bloom, F. R. ( 1991; ). Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol 204, 63–113.
    [Google Scholar]
  12. Hedegaard, L. & Danchin, A. ( 1985; ). The cya gene region of Erwinia chrysanthemi B374: organisation and gene products. Mol Gen Genet 201, 38–42.[CrossRef]
    [Google Scholar]
  13. Helmann, J. D. & Moran, C. P. J. ( 2002; ). RNA polymerase and sigma factors. In Bacillus subtilis and its Closest Relatives: from Genes to Cells, pp. 289–312. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
  14. Horsburgh, M. J. & Moir, A. ( 1999; ). σ M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol Microbiol 32, 41–50.[CrossRef]
    [Google Scholar]
  15. Hulett, F. M. ( 2002; ). The Pho regulon. In Bacillus subtilis and its Closest Relatives: from Genes to Cells, pp. 193–201. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
  16. Karamata, D. & Gross, J. D. ( 1970; ). Isolation and genetic analysis of temperature-sensitive mutants of Bacillus subtilis defective in DNA synthesis. Mol Gen Genet 108, 277–287.
    [Google Scholar]
  17. Karamata, D., Pooley, H. M. & Monod, M. ( 1987; ). Expression of heterologous genes for wall teichoic acid in Bacillus subtilis 168. Mol Gen Genet 207, 73–81.[CrossRef]
    [Google Scholar]
  18. Lazarevic, V., Abellan, F.-X., Beggah Moller, S., Karamata, D. & Mauël, C. ( 2002a; ). Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology 148, 815–824.
    [Google Scholar]
  19. Lazarevic, V., Pooley, H. M., Mauël, C. & Karamata, D. ( 2002b; ). Teichoic and teichuronic acids from Gram-positive bacteria. In Polysaccharides I. Polysaccharides from Prokaryotes, vol. 5, pp. 465–492. Edited by A. Steinbüchel, E. J. Vandamme & S. de Baets. Weinheim: Wiley-VCH.
  20. Liu, W., Eder, S. & Hulett, F. M. ( 1998; ). Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role for PhoP-P. J Bacteriol 180, 753–758.
    [Google Scholar]
  21. Mascher, T., Margulis, N. G., Wang, T., Ye, R. W. & Helmann, J. D. ( 2003; ). Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol Microbiol 50, 1591–1604.[CrossRef]
    [Google Scholar]
  22. Mauël, C., Young, M., Margot, P. & Karamata, D. ( 1989; ). The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis. Mol Gen Genet 215, 388–394.[CrossRef]
    [Google Scholar]
  23. Mauël, C., Young, M., Monsutti-Grecescu, A., Marriott, S. A. & Karamata, D. ( 1994; ). Analysis of Bacillus subtilis tag gene expression using transcriptional fusions. Microbiology 140, 2279–2288.[CrossRef]
    [Google Scholar]
  24. Miller, J. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  25. Minnig, K., Barblan, J.-L., Kehl, S., Beggah Möller, S. & Mauël, C. ( 2003; ). In Bacillus subtilis W23, the duet σ X σ M, two sigma factors of the extracytoplasmic function subfamily, are required for septum and cell wall synthesis under batch culture conditions. Mol Microbiol 49, 1435–1447.[CrossRef]
    [Google Scholar]
  26. Müller, J. P., An, Z., Merad, T., Hancock, I. C. & Harwood, C. R. ( 1997; ). Influence of Bacillus subtilis phoR on cell wall anionic polymers. Microbiology 143, 947–956.[CrossRef]
    [Google Scholar]
  27. Price, C. W., Fawcett, P., Cérémonie, H., Su, N., Murphy, C. K. & Youngman, P. ( 2001; ). Genome-wide analysis of the general stress response in Bacillus subtilis. Mol Microbiol 41, 757–774.
    [Google Scholar]
  28. Qi, Y. & Hulett, F. M. ( 1998; ). Role of PhoP-P in transcriptional regulation of genes involved in cell wall anionic polymer synthesis in Bacillus subtilis. J Bacteriol 180, 4007–4010.
    [Google Scholar]
  29. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  30. Soldo, B., Lazarevic, V., Pagni, M. & Karamata, D. ( 1999; ). Teichuronic acid operon of Bacillus subtilis 168. Mol Microbiol 31, 795–805.[CrossRef]
    [Google Scholar]
  31. Soldo, B., Lazarevic, V. & Karamata, D. ( 2002; ). tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148, 2079–2087.
    [Google Scholar]
  32. Thackray, P. D. & Moir, A. ( 2003; ). SigM, an extracytoplasmic function sigma factor of Bacillus subtilis, is activated in response to cell wall antibiotics, ethanol, heat, acid, and superoxide stress. J Bacteriol 185, 3491–3498.[CrossRef]
    [Google Scholar]
  33. Wright, J. & Heckels, J. E. ( 1975; ). The teichuronic acid of cell walls of Bacillus subtilis W23 grown in a chemostat under phosphate limitation. Biochem J 147, 187–189.
    [Google Scholar]
  34. Yanisch-Perron, C., Vieira, J. & Messing, J. ( 1985; ). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103–119.[CrossRef]
    [Google Scholar]
  35. Young, F. E. ( 1966; ). Fractionation and partial characterization of the products of autolysis of cell walls of Bacillus subtilis. J Bacteriol 92, 839–846.
    [Google Scholar]
  36. Young, M., Mauël, C., Margot, P. & Karamata, D. ( 1989; ). Pseudo-allelic relationship between non-homologous genes concerned with biosynthesis of polyglycerol phosphate and polyribitol phosphate teichoic acids in Bacillus subtilis strains 168 and W23. Mol Microbiol 3, 1805–1812.[CrossRef]
    [Google Scholar]
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