Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Oct;178(20):5910–5915. doi: 10.1128/jb.178.20.5910-5915.1996

CodY is required for nutritional repression of Bacillus subtilis genetic competence.

P Serror 1, A L Sonenshein 1
PMCID: PMC178446  PMID: 8830686

Abstract

The acquisition of genetic competence by Bacillus subtilis is repressed when the growth medium contains Casamino Acids. This repression was shown to be exerted at the level of expression from the promoters of the competence-regulatory genes srfA and comK and was relieved in strains carrying a null mutation in the codY gene. DNase I footprinting experiments showed that purified CodY binds directly to the srfA and comK promoter regions.

Full Text

The Full Text of this article is available as a PDF (681.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albano M., Hahn J., Dubnau D. Expression of competence genes in Bacillus subtilis. J Bacteriol. 1987 Jul;169(7):3110–3117. doi: 10.1128/jb.169.7.3110-3117.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Atkinson M. R., Fisher S. H. Identification of genes and gene products whose expression is activated during nitrogen-limited growth in Bacillus subtilis. J Bacteriol. 1991 Jan;173(1):23–27. doi: 10.1128/jb.173.1.23-27.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atkinson M. R., Wray L. V., Jr, Fisher S. H. Regulation of histidine and proline degradation enzymes by amino acid availability in Bacillus subtilis. J Bacteriol. 1990 Sep;172(9):4758–4765. doi: 10.1128/jb.172.9.4758-4765.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belitsky B. R., Janssen P. J., Sonenshein A. L. Sites required for GltC-dependent regulation of Bacillus subtilis glutamate synthase expression. J Bacteriol. 1995 Oct;177(19):5686–5695. doi: 10.1128/jb.177.19.5686-5695.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. D'Souza C., Nakano M. M., Corbell N., Zuber P. Amino-acylation site mutations in amino acid-activating domains of surfactin synthetase: effects on surfactin production and competence development in Bacillus subtilis. J Bacteriol. 1993 Jun;175(11):3502–3510. doi: 10.1128/jb.175.11.3502-3510.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. D'Souza C., Nakano M. M., Zuber P. Identification of comS, a gene of the srfA operon that regulates the establishment of genetic competence in Bacillus subtilis. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9397–9401. doi: 10.1073/pnas.91.20.9397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dubnau D., Davidoff-Abelson R. Fate of transforming DNA following uptake by competent Bacillus subtilis. I. Formation and properties of the donor-recipient complex. J Mol Biol. 1971 Mar 14;56(2):209–221. doi: 10.1016/0022-2836(71)90460-8. [DOI] [PubMed] [Google Scholar]
  8. Dubnau D., Roggiani M. Growth medium-independent genetic competence mutants of Bacillus subtilis. J Bacteriol. 1990 Jul;172(7):4048–4055. doi: 10.1128/jb.172.7.4048-4055.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fisher S. H., Rohrer K., Ferson A. E. Role of CodY in regulation of the Bacillus subtilis hut operon. J Bacteriol. 1996 Jul;178(13):3779–3784. doi: 10.1128/jb.178.13.3779-3784.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fouet A., Sonenshein A. L. A target for carbon source-dependent negative regulation of the citB promoter of Bacillus subtilis. J Bacteriol. 1990 Feb;172(2):835–844. doi: 10.1128/jb.172.2.835-844.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grossman A. D. Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu Rev Genet. 1995;29:477–508. doi: 10.1146/annurev.ge.29.120195.002401. [DOI] [PubMed] [Google Scholar]
  12. Guillen N., Weinrauch Y., Dubnau D. A. Cloning and characterization of the regulatory Bacillus subtilis competence genes comA and comB. J Bacteriol. 1989 Oct;171(10):5354–5361. doi: 10.1128/jb.171.10.5354-5361.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hahn J., Dubnau D. Growth stage signal transduction and the requirements for srfA induction in development of competence. J Bacteriol. 1991 Nov;173(22):7275–7282. doi: 10.1128/jb.173.22.7275-7282.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hahn J., Kong L., Dubnau D. The regulation of competence transcription factor synthesis constitutes a critical control point in the regulation of competence in Bacillus subtilis. J Bacteriol. 1994 Sep;176(18):5753–5761. doi: 10.1128/jb.176.18.5753-5761.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hamoen L. W., Eshuis H., Jongbloed J., Venema G., van Sinderen D. A small gene, designated comS, located within the coding region of the fourth amino acid-activation domain of srfA, is required for competence development in Bacillus subtilis. Mol Microbiol. 1995 Jan;15(1):55–63. doi: 10.1111/j.1365-2958.1995.tb02220.x. [DOI] [PubMed] [Google Scholar]
  16. Kong L., Dubnau D. Regulation of competence-specific gene expression by Mec-mediated protein-protein interaction in Bacillus subtilis. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5793–5797. doi: 10.1073/pnas.91.13.5793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kong L., Siranosian K. J., Grossman A. D., Dubnau D. Sequence and properties of mecA, a negative regulator of genetic competence in Bacillus subtilis. Mol Microbiol. 1993 Jul;9(2):365–373. doi: 10.1111/j.1365-2958.1993.tb01697.x. [DOI] [PubMed] [Google Scholar]
  18. Magnuson R., Solomon J., Grossman A. D. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell. 1994 Apr 22;77(2):207–216. doi: 10.1016/0092-8674(94)90313-1. [DOI] [PubMed] [Google Scholar]
  19. Mathiopoulos C., Mueller J. P., Slack F. J., Murphy C. G., Patankar S., Bukusoglu G., Sonenshein A. L. A Bacillus subtilis dipeptide transport system expressed early during sporulation. Mol Microbiol. 1991 Aug;5(8):1903–1913. doi: 10.1111/j.1365-2958.1991.tb00814.x. [DOI] [PubMed] [Google Scholar]
  20. Msadek T., Kunst F., Rapoport G. MecB of Bacillus subtilis, a member of the ClpC ATPase family, is a pleiotropic regulator controlling competence gene expression and growth at high temperature. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5788–5792. doi: 10.1073/pnas.91.13.5788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mueller J. P., Bukusoglu G., Sonenshein A. L. Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol. 1992 Jul;174(13):4361–4373. doi: 10.1128/jb.174.13.4361-4373.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nakano M. M., Xia L. A., Zuber P. Transcription initiation region of the srfA operon, which is controlled by the comP-comA signal transduction system in Bacillus subtilis. J Bacteriol. 1991 Sep;173(17):5487–5493. doi: 10.1128/jb.173.17.5487-5493.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nakano M. M., Zuber P. The primary role of comA in establishment of the competent state in Bacillus subtilis is to activate expression of srfA. J Bacteriol. 1991 Nov;173(22):7269–7274. doi: 10.1128/jb.173.22.7269-7274.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Perego M., Hanstein C., Welsh K. M., Djavakhishvili T., Glaser P., Hoch J. A. Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell. 1994 Dec 16;79(6):1047–1055. doi: 10.1016/0092-8674(94)90035-3. [DOI] [PubMed] [Google Scholar]
  25. Perego M., Higgins C. F., Pearce S. R., Gallagher M. P., Hoch J. A. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol. 1991 Jan;5(1):173–185. doi: 10.1111/j.1365-2958.1991.tb01838.x. [DOI] [PubMed] [Google Scholar]
  26. Perego M., Spiegelman G. B., Hoch J. A. Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol Microbiol. 1988 Nov;2(6):689–699. doi: 10.1111/j.1365-2958.1988.tb00079.x. [DOI] [PubMed] [Google Scholar]
  27. Roggiani M., Dubnau D. ComA, a phosphorylated response regulator protein of Bacillus subtilis, binds to the promoter region of srfA. J Bacteriol. 1993 May;175(10):3182–3187. doi: 10.1128/jb.175.10.3182-3187.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rudner D. Z., LeDeaux J. R., Ireton K., Grossman A. D. The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J Bacteriol. 1991 Feb;173(4):1388–1398. doi: 10.1128/jb.173.4.1388-1398.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Serror P., Sonenshein A. L. Interaction of CodY, a novel Bacillus subtilis DNA-binding protein, with the dpp promoter region. Mol Microbiol. 1996 May;20(4):843–852. doi: 10.1111/j.1365-2958.1996.tb02522.x. [DOI] [PubMed] [Google Scholar]
  30. Slack F. J., Mueller J. P., Sonenshein A. L. Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon. J Bacteriol. 1993 Aug;175(15):4605–4614. doi: 10.1128/jb.175.15.4605-4614.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Slack F. J., Mueller J. P., Strauch M. A., Mathiopoulos C., Sonenshein A. L. Transcriptional regulation of a Bacillus subtilis dipeptide transport operon. Mol Microbiol. 1991 Aug;5(8):1915–1925. doi: 10.1111/j.1365-2958.1991.tb00815.x. [DOI] [PubMed] [Google Scholar]
  32. Slack F. J., Serror P., Joyce E., Sonenshein A. L. A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol Microbiol. 1995 Feb;15(4):689–702. doi: 10.1111/j.1365-2958.1995.tb02378.x. [DOI] [PubMed] [Google Scholar]
  33. Solomon J. M., Magnuson R., Srivastava A., Grossman A. D. Convergent sensing pathways mediate response to two extracellular competence factors in Bacillus subtilis. Genes Dev. 1995 Mar 1;9(5):547–558. doi: 10.1101/gad.9.5.547. [DOI] [PubMed] [Google Scholar]
  34. Steinmetz M., Richter R. Plasmids designed to alter the antibiotic resistance expressed by insertion mutations in Bacillus subtilis, through in vivo recombination. Gene. 1994 May 3;142(1):79–83. doi: 10.1016/0378-1119(94)90358-1. [DOI] [PubMed] [Google Scholar]
  35. Vasantha N., Freese E. Enzyme changes during Bacillus subtilis sporulation caused by deprivation of guanine nucleotides. J Bacteriol. 1980 Dec;144(3):1119–1125. doi: 10.1128/jb.144.3.1119-1125.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. YOUNG F. E., SPIZIZEN J. Physiological and genetic factors affecting transformation of Bacillus subtilis. J Bacteriol. 1961 May;81:823–829. doi: 10.1128/jb.81.5.823-829.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. van Sinderen D., Luttinger A., Kong L., Dubnau D., Venema G., Hamoen L. comK encodes the competence transcription factor, the key regulatory protein for competence development in Bacillus subtilis. Mol Microbiol. 1995 Feb;15(3):455–462. doi: 10.1111/j.1365-2958.1995.tb02259.x. [DOI] [PubMed] [Google Scholar]
  38. van Sinderen D., Venema G. comK acts as an autoregulatory control switch in the signal transduction route to competence in Bacillus subtilis. J Bacteriol. 1994 Sep;176(18):5762–5770. doi: 10.1128/jb.176.18.5762-5770.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. van Sinderen D., Withoff S., Boels H., Venema G. Isolation and characterization of comL, a transcription unit involved in competence development of Bacillus subtilis. Mol Gen Genet. 1990 Dec;224(3):396–404. doi: 10.1007/BF00262434. [DOI] [PubMed] [Google Scholar]
  40. van Sinderen D., ten Berge A., Hayema B. J., Hamoen L., Venema G. Molecular cloning and sequence of comK, a gene required for genetic competence in Bacillus subtilis. Mol Microbiol. 1994 Feb;11(4):695–703. doi: 10.1111/j.1365-2958.1994.tb00347.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES