The Bacillus Subtilis Sigma(M) Regulon and Its Contribution to Cell Envelope Stress Responses

Overview

Journal Mol Microbiol

Specialties Microbiology
Molecular Biology

Date 2008 Jan 9

PMID 18179421

Citations 114

Authors

Warawan Eiamphungporn

John D Helmann

Affiliations

Soon will be listed here.

Abstract

The Bacillus subtilis extracytoplasmic function (ECF) sigma(M) factor is activated by cell envelope stress elicited by antibiotics, and by acid, heat, ethanol and superoxide stresses. Here, we have used several complementary approaches to identify genes controlled by sigma(M). In many cases, expression is only partially dependent on sigma(M) because of both overlapping promoter recognition with other ECF sigma factors and the presence of additional promoter elements. Genes regulated by sigma(M) have a characteristic pattern of induction in response to cell envelope-acting antibiotics as evidenced by hierarchical clustering analysis. sigma(M) also contributes to the expression of the Spx transcription factor and thereby indirectly regulates genes of the Spx regulon. Cell envelope stress responses also include regulons controlled by sigma(W), sigma(B) and several two-component regulatory systems (e.g. LiaRS, YycFG, BceRS). Activation of the sigma(M) regulon increases expression of proteins functioning in transcriptional control, cell wall synthesis and shape determination, cell division, DNA damage monitoring, recombinational repair and detoxification.

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References

Raivio T, Silhavy T . Periplasmic stress and ECF sigma factors. Annu Rev Microbiol. 2001; 55:591-624. DOI: 10.1146/annurev.micro.55.1.591. View

Harry E, Rowland S, Malo M, Wake R . Expression of divIB of Bacillus subtilis during vegetative growth. J Bacteriol. 1994; 176(4):1172-9. PMC: 205170. DOI: 10.1128/jb.176.4.1172-1179.1994. View

Henriques A, Glaser P, Piggot P, Moran Jr C . Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol. 1998; 28(2):235-47. DOI: 10.1046/j.1365-2958.1998.00766.x. View

Huang X, Helmann J . Identification of target promoters for the Bacillus subtilis sigma X factor using a consensus-directed search. J Mol Biol. 1998; 279(1):165-73. DOI: 10.1006/jmbi.1998.1765. View

Huang X, Fredrick K, Helmann J . Promoter recognition by Bacillus subtilis sigmaW: autoregulation and partial overlap with the sigmaX regulon. J Bacteriol. 1998; 180(15):3765-70. PMC: 107356. DOI: 10.1128/JB.180.15.3765-3770.1998. View

Bolhuis A, Broekhuizen C, Sorokin A, van Roosmalen M, Venema G, Bron S . SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins. J Biol Chem. 1998; 273(33):21217-24. DOI: 10.1074/jbc.273.33.21217. View

Eisen M, Spellman P, Brown P, Botstein D . Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998; 95(25):14863-8. PMC: 24541. DOI: 10.1073/pnas.95.25.14863. View

Huang X, Gaballa A, Cao M, Helmann J . Identification of target promoters for the Bacillus subtilis extracytoplasmic function sigma factor, sigma W. Mol Microbiol. 1999; 31(1):361-71. DOI: 10.1046/j.1365-2958.1999.01180.x. View

Horsburgh M, Moir A . Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol Microbiol. 1999; 32(1):41-50. DOI: 10.1046/j.1365-2958.1999.01323.x. View

10.

Petersohn A, Bernhardt J, Gerth U, Hoper D, Koburger T, Volker U . Identification of sigma(B)-dependent genes in Bacillus subtilis using a promoter consensus-directed search and oligonucleotide hybridization. J Bacteriol. 1999; 181(18):5718-24. PMC: 94092. DOI: 10.1128/JB.181.18.5718-5724.1999. View

11.

Nakano S, Erwin K, Ralle M, Zuber P . Redox-sensitive transcriptional control by a thiol/disulphide switch in the global regulator, Spx. Mol Microbiol. 2005; 55(2):498-510. DOI: 10.1111/j.1365-2958.2004.04395.x. View

12.

Borukhov S, Lee J, Laptenko O . Bacterial transcription elongation factors: new insights into molecular mechanism of action. Mol Microbiol. 2005; 55(5):1315-24. DOI: 10.1111/j.1365-2958.2004.04481.x. View

13.

Cao M, Moore C, Helmann J . Bacillus subtilis paraquat resistance is directed by sigmaM, an extracytoplasmic function sigma factor, and is conferred by YqjL and BcrC. J Bacteriol. 2005; 187(9):2948-56. PMC: 1082808. DOI: 10.1128/JB.187.9.2948-2956.2005. View

14.

Hyyrylainen H, Sarvas M, Kontinen V . Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl Microbiol Biotechnol. 2005; 67(3):389-96. DOI: 10.1007/s00253-005-1898-1. View

15.

Cao M, Helmann J . Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors. J Bacteriol. 2002; 184(22):6123-9. PMC: 151963. DOI: 10.1128/JB.184.22.6123-6129.2002. View

16.

Ohki R, Tateno K, Okada Y, Okajima H, Asai K, Sadaie Y . A bacitracin-resistant Bacillus subtilis gene encodes a homologue of the membrane-spanning subunit of the Bacillus licheniformis ABC transporter. J Bacteriol. 2002; 185(1):51-9. PMC: 141914. DOI: 10.1128/JB.185.1.51-59.2003. View

17.

Errington J, Daniel R, Scheffers D . Cytokinesis in bacteria. Microbiol Mol Biol Rev. 2003; 67(1):52-65, table of contents. PMC: 150516. DOI: 10.1128/MMBR.67.1.52-65.2003. View

18.

Asai K, Yamaguchi H, Kang C, Yoshida K, Fujita Y, Sadaie Y . DNA microarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett. 2003; 220(1):155-60. DOI: 10.1016/S0378-1097(03)00093-4. View

19.

Nakano S, Nakano M, Zhang Y, Leelakriangsak M, Zuber P . A regulatory protein that interferes with activator-stimulated transcription in bacteria. Proc Natl Acad Sci U S A. 2003; 100(7):4233-8. PMC: 153076. DOI: 10.1073/pnas.0637648100. View

20.

Thackray P, Moir A . 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. 2003; 185(12):3491-8. PMC: 156226. DOI: 10.1128/JB.185.12.3491-3498.2003. View