Abstract
sigma B is a secondary sigma factor of Bacillus subtilis. sigma B-dependent transcription is induced when B. subtilis enters the stationary phase of growth or is exposed to any of a number of different environmental stresses. Three genes (rsbV, rsbW, and rsbX), which are cotranscribed with the sigma B structural gene (sigB), encode regulators of sigma B-dependent gene expression. RsbW and RsbV have been shown to control sigma B activity, functioning as an inhibitory sigma B binding protein and its antagonist, respectively. Using the SPAC promoter (PSPAC) to control the expression of the sigB operon, a ctc::lacZ reporter system to monitor sigma B activity, and monoclonal antibodies to determine the levels of sigB operon products, we have now obtained evidence that RsbX is an indirect regulator of sigma B activity. Genetic data and in vivo measurements argue that RsbX negatively regulates an extension of the RsbV-RsbW pathway that requires the product of an additional regulatory gene (rsbU) which lies immediately upstream of the sigB operon. The results are consistent with RsbU, or a process dependent on RsbU, being able to facilitate the RsbV-dependent release of sigma B from RsbW but normally prevented from doing this by RsbX.
Full Text
The Full Text of this article is available as a PDF (551.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alper S., Duncan L., Losick R. An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in B. subtilis. Cell. 1994 Apr 22;77(2):195–205. doi: 10.1016/0092-8674(94)90312-3. [DOI] [PubMed] [Google Scholar]
- Benson A. K., Haldenwang W. G. Bacillus subtilis sigma B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2330–2334. doi: 10.1073/pnas.90.6.2330. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benson A. K., Haldenwang W. G. Characterization of a regulatory network that controls sigma B expression in Bacillus subtilis. J Bacteriol. 1992 Feb;174(3):749–757. doi: 10.1128/jb.174.3.749-757.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benson A. K., Haldenwang W. G. Regulation of sigma B levels and activity in Bacillus subtilis. J Bacteriol. 1993 Apr;175(8):2347–2356. doi: 10.1128/jb.175.8.2347-2356.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benson A. K., Haldenwang W. G. The sigma B-dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J Bacteriol. 1993 Apr;175(7):1929–1935. doi: 10.1128/jb.175.7.1929-1935.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Binnie C., Lampe M., Losick R. Gene encoding the sigma 37 species of RNA polymerase sigma factor from Bacillus subtilis. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5943–5947. doi: 10.1073/pnas.83.16.5943. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boylan S. A., Redfield A. R., Brody M. S., Price C. W. Stress-induced activation of the sigma B transcription factor of Bacillus subtilis. J Bacteriol. 1993 Dec;175(24):7931–7937. doi: 10.1128/jb.175.24.7931-7937.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boylan S. A., Redfield A. R., Price C. W. Transcription factor sigma B of Bacillus subtilis controls a large stationary-phase regulon. J Bacteriol. 1993 Jul;175(13):3957–3963. doi: 10.1128/jb.175.13.3957-3963.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boylan S. A., Rutherford A., Thomas S. M., Price C. W. Activation of Bacillus subtilis transcription factor sigma B by a regulatory pathway responsive to stationary-phase signals. J Bacteriol. 1992 Jun;174(11):3695–3706. doi: 10.1128/jb.174.11.3695-3706.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boylan S. A., Thomas M. D., Price C. W. Genetic method to identify regulons controlled by nonessential elements: isolation of a gene dependent on alternate transcription factor sigma B of Bacillus subtilis. J Bacteriol. 1991 Dec;173(24):7856–7866. doi: 10.1128/jb.173.24.7856-7866.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dufour A., Haldenwang W. G. Interactions between a Bacillus subtilis anti-sigma factor (RsbW) and its antagonist (RsbV). J Bacteriol. 1994 Apr;176(7):1813–1820. doi: 10.1128/jb.176.7.1813-1820.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duncan L., Losick R. SpoIIAB is an anti-sigma factor that binds to and inhibits transcription by regulatory protein sigma F from Bacillus subtilis. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2325–2329. doi: 10.1073/pnas.90.6.2325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duncan M. L., Kalman S. S., Thomas S. M., Price C. W. Gene encoding the 37,000-dalton minor sigma factor of Bacillus subtilis RNA polymerase: isolation, nucleotide sequence, chromosomal locus, and cryptic function. J Bacteriol. 1987 Feb;169(2):771–778. doi: 10.1128/jb.169.2.771-778.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haldenwang W. G., Losick R. Novel RNA polymerase sigma factor from Bacillus subtilis. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7000–7004. doi: 10.1073/pnas.77.12.7000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Igo M. M., Losick R. Regulation of a promoter that is utilized by minor forms of RNA polymerase holoenzyme in Bacillus subtilis. J Mol Biol. 1986 Oct 20;191(4):615–624. doi: 10.1016/0022-2836(86)90449-3. [DOI] [PubMed] [Google Scholar]
- Igo M., Lampe M., Ray C., Schafer W., Moran C. P., Jr, Losick R. Genetic studies of a secondary RNA polymerase sigma factor in Bacillus subtilis. J Bacteriol. 1987 Aug;169(8):3464–3469. doi: 10.1128/jb.169.8.3464-3469.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalman S., Duncan M. L., Thomas S. M., Price C. W. Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase. J Bacteriol. 1990 Oct;172(10):5575–5585. doi: 10.1128/jb.172.10.5575-5585.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kenney T. J., Moran C. P., Jr Organization and regulation of an operon that encodes a sporulation-essential sigma factor in Bacillus subtilis. J Bacteriol. 1987 Jul;169(7):3329–3339. doi: 10.1128/jb.169.7.3329-3339.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kirchman P. A., DeGrazia H., Kellner E. M., Moran C. P., Jr Forespore-specific disappearance of the sigma-factor antagonist spoIIAB: implications for its role in determination of cell fate in Bacillus subtilis. Mol Microbiol. 1993 May;8(4):663–671. doi: 10.1111/j.1365-2958.1993.tb01610.x. [DOI] [PubMed] [Google Scholar]
- Min K. T., Hilditch C. M., Diederich B., Errington J., Yudkin M. D. Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. Cell. 1993 Aug 27;74(4):735–742. doi: 10.1016/0092-8674(93)90520-z. [DOI] [PubMed] [Google Scholar]
- Rather P. N., Coppolecchia R., DeGrazia H., Moran C. P., Jr Negative regulator of sigma G-controlled gene expression in stationary-phase Bacillus subtilis. J Bacteriol. 1990 Feb;172(2):709–715. doi: 10.1128/jb.172.2.709-715.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmidt R., Margolis P., Duncan L., Coppolecchia R., Moran C. P., Jr, Losick R. Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9221–9225. doi: 10.1073/pnas.87.23.9221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Varón D., Boylan S. A., Okamoto K., Price C. W. Bacillus subtilis gtaB encodes UDP-glucose pyrophosphorylase and is controlled by stationary-phase transcription factor sigma B. J Bacteriol. 1993 Jul;175(13):3964–3971. doi: 10.1128/jb.175.13.3964-3971.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Völker U., Engelmann S., Maul B., Riethdorf S., Völker A., Schmid R., Mach H., Hecker M. Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology. 1994 Apr;140(Pt 4):741–752. doi: 10.1099/00221287-140-4-741. [DOI] [PubMed] [Google Scholar]
- Wise A. A., Price C. W. Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor sigma B in response to environmental signals. J Bacteriol. 1995 Jan;177(1):123–133. doi: 10.1128/jb.177.1.123-133.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yansura D. G., Henner D. J. Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis. Proc Natl Acad Sci U S A. 1984 Jan;81(2):439–443. doi: 10.1073/pnas.81.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yasbin R. E., Wilson G. A., Young F. E. Transformation and transfection in lysogenic strains of Bacillus subtilis 168. J Bacteriol. 1973 Feb;113(2):540–548. doi: 10.1128/jb.113.2.540-548.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]