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Chapter 17 : General Stress Response in and Related Gram-Positive Bacteria

Author: Chester W. Price1
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Affiliations: 1: Department of Microbiology, University of California at Davis, Davis, CA 95616
Content Type: Monograph
Publication Year: 2011

Category: Microbial Genetics and Molecular Biology

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Abstract:

This chapter focuses on the partner-switching mechanism, showing how signaling versatility is achieved and outlining the questions about network function that remain to be answered. A short section at the end of the chapter summarizes the roles of general stress regulons in the physiology of gram-positive organisms that possess s, or σ-like factors. In , RsbW has two activities in unstressed cells: (i) as an anti-sigma factor it binds σ and prevents its association with RNA polymerase; and (ii) as a serine kinase it specifically phosphorylates and inactivates its own antagonist, the RsbV anti- anti-sigma. Three single-domain anti-anti- sigma factors of have atypical N-terminal extensions rich in serine and threonine residues, allowing their interactions to be controlled by a unique mechanism that may affect σ activity. In many gram-positive bacteria σ is a master regulator of a general stress modulon that closely interacts with other global systems. Investigation of the roles of genes in the modulon can provide a unique perspective regarding the physiological changes that promote stress resistance. How σ signaling networks sense activating stresses remains an open question. Given the wide distribution of the recognized sensing modules and their association with different output domains, this question is relevant to many signaling pathways.

Citation: Price C. 2011. General Stress Response in and Related Gram-Positive Bacteria, p 301-318. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch17

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General Stress Response in Bacillus subtilis and Related Gram-Positive Bacteria
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Citation: Price C. 2011. General Stress Response in and Related Gram-Positive Bacteria, p 301-318. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch17
/content/10.1128/9781555816841.ch17.ch17fig01
Figure 1.
σ regulatory network in . (A) Genes encoding the principal network regulators are organized in two operons. Energy regulators (RsbQ and P) are indicated by light stippling; environmental regulators (RsbRA, S, T, U, and X) by dark; and common regulators (RsbV and W) by white. Promoters are denoted by the holoenzyme known (or likely) to recognize them. Other RsbR paralogs and the YtvA blue light sensor are encoded in scattered transcriptional units (not shown). (B) Model of the signaling network. Energy and environmental pathways converge on RsbV and RsbW, which directly regulate σ activity (see text). Horizontal arrows show conversion between RsbV and RsbV-P (with phosphate as stippled P). Full arrowheads indicate activating effects and T-headed lines inhibiting ones. PAS and N denote the regulatory domains of RsbP and RsbU, respectively. A cold stress input that bypasses these established pathways is less well understood. (C) Model of the environmental pathway that activates the RsbU phosphatase. The stressosome complex is represented by the RsbRA co-antagonist and RsbS antagonist. RsbRB, RC, RD, and YtvA are also present within the complex (not shown). Symbols are as in panel B.
10.1128/9781555816841/f0303-01_thmb.gif
10.1128/9781555816841/f0303-01.gif
Image of Figure 1.
Figure 1.

σ regulatory network in . (A) Genes encoding the principal network regulators are organized in two operons. Energy regulators (RsbQ and P) are indicated by light stippling; environmental regulators (RsbRA, S, T, U, and X) by dark; and common regulators (RsbV and W) by white. Promoters are denoted by the holoenzyme known (or likely) to recognize them. Other RsbR paralogs and the YtvA blue light sensor are encoded in scattered transcriptional units (not shown). (B) Model of the signaling network. Energy and environmental pathways converge on RsbV and RsbW, which directly regulate σ activity (see text). Horizontal arrows show conversion between RsbV and RsbV-P (with phosphate as stippled P). Full arrowheads indicate activating effects and T-headed lines inhibiting ones. PAS and N denote the regulatory domains of RsbP and RsbU, respectively. A cold stress input that bypasses these established pathways is less well understood. (C) Model of the environmental pathway that activates the RsbU phosphatase. The stressosome complex is represented by the RsbRA co-antagonist and RsbS antagonist. RsbRB, RC, RD, and YtvA are also present within the complex (not shown). Symbols are as in panel B.

Citation: Price C. 2011. General Stress Response in and Related Gram-Positive Bacteria, p 301-318. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch17
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Figure 2.
Model of energy-stress signaling. The RsbP phosphatase and RsbW kinase provide two potential inputs to regulate the energy stress response (see text). Domains shown are involved in signaling; conversion, activating, and inhibiting symbols are as per Fig. 1 legend. RsbP input: the labels A and A’ indicate the hypothetical small molecule substrate and product of the RsbQ hydrolase; A’ is thought to bind the PAS domain of RsbP. PAS then activates the PP2C phosphatase domain by countering the negative effect of the coiled-coil. RsbW input: kinase activity increases in energy sufficient cells and decreases in starved cells, leading to diminished phosphorylation of the STAS domain of RsbV.
10.1128/9781555816841/f0304-01_thmb.gif
10.1128/9781555816841/f0304-01.gif
Image of Figure 2.
Figure 2.

Model of energy-stress signaling. The RsbP phosphatase and RsbW kinase provide two potential inputs to regulate the energy stress response (see text). Domains shown are involved in signaling; conversion, activating, and inhibiting symbols are as per Fig. 1 legend. RsbP input: the labels A and A’ indicate the hypothetical small molecule substrate and product of the RsbQ hydrolase; A’ is thought to bind the PAS domain of RsbP. PAS then activates the PP2C phosphatase domain by countering the negative effect of the coiled-coil. RsbW input: kinase activity increases in energy sufficient cells and decreases in starved cells, leading to diminished phosphorylation of the STAS domain of RsbV.

Citation: Price C. 2011. General Stress Response in and Related Gram-Positive Bacteria, p 301-318. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch17
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Figure 3.
Model of environmental-stress signaling. RsbRA and RsbS form the core of the stressosome complex, which binds the RsbT kinase in an inactive state. For simplicity, the functional RsbRA dimer is represented here as a monomer, with its N-terminal nonheme globin domain (RNTD) and C-terminal STAS domain (RCTD) joined via a 13-residue α-helical linker (solid line). The smaller RsbS (S) has only a STAS domain, which directly binds RsbT (T). In this model, a stress signal results in a structural perturbation within RNTD. The perturbation is communicated via the α-helical linker to RCTD and thence to the adjacent S. These structural changes in the STAS domains of R and S allow their phosphorylation by T, which is then released to activate the RsbU phosphatase. In vivo the core of each stressosome consists of a mix of the RsbR family members RsbRA, RB, RC, RD, and YtvA, together with RsbS.
10.1128/9781555816841/f0307-01_thmb.gif
10.1128/9781555816841/f0307-01.gif
Image of Figure 3.
Figure 3.

Model of environmental-stress signaling. RsbRA and RsbS form the core of the stressosome complex, which binds the RsbT kinase in an inactive state. For simplicity, the functional RsbRA dimer is represented here as a monomer, with its N-terminal nonheme globin domain (RNTD) and C-terminal STAS domain (RCTD) joined via a 13-residue α-helical linker (solid line). The smaller RsbS (S) has only a STAS domain, which directly binds RsbT (T). In this model, a stress signal results in a structural perturbation within RNTD. The perturbation is communicated via the α-helical linker to RCTD and thence to the adjacent S. These structural changes in the STAS domains of R and S allow their phosphorylation by T, which is then released to activate the RsbU phosphatase. In vivo the core of each stressosome consists of a mix of the RsbR family members RsbRA, RB, RC, RD, and YtvA, together with RsbS.

Citation: Price C. 2011. General Stress Response in and Related Gram-Positive Bacteria, p 301-318. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch17
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Figure 4.
Comparison of operons and functionally associated regulatory factors in gram-positive bacteria. Promoters are indicated by the holoenzyme form known or proposed to recognize them. Lm, ; Sa, ; Bc, ; Mt, ; Sc, . The Lm operon is organized like its counterpart; dark stippling indicates known or suspected environmental regulators. Lm has additional RsbR paralogs and a YtvA blue light ortholog encoded elsewhere on the genome (not shown); these are presumed to form a stressosome complex with RsbRA and RsbS. Mt and Sc likewise have numerous potential regulators, but only those tested for a direct effect on sigma activity are included here (see text).
10.1128/9781555816841/f0309-01_thmb.gif
10.1128/9781555816841/f0309-01.gif
Image of Figure 4.
Figure 4.

Comparison of operons and functionally associated regulatory factors in gram-positive bacteria. Promoters are indicated by the holoenzyme form known or proposed to recognize them. Lm, ; Sa, ; Bc, ; Mt, ; Sc, . The Lm operon is organized like its counterpart; dark stippling indicates known or suspected environmental regulators. Lm has additional RsbR paralogs and a YtvA blue light ortholog encoded elsewhere on the genome (not shown); these are presumed to form a stressosome complex with RsbRA and RsbS. Mt and Sc likewise have numerous potential regulators, but only those tested for a direct effect on sigma activity are included here (see text).

Citation: Price C. 2011. General Stress Response in and Related Gram-Positive Bacteria, p 301-318. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch17
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References

/content/book/10.1128/9781555816841.ch17
1. Akbar,, S.,, C. M. Kang,, T. A. Gaidenko, and, C. W. Price. 1997. Modulator protein RsbR regulates environmental signalling in the general stress pathway of Bacillus subtilis. Mol. Microbiol. 24: 567– 578.
2. Allenby,, N. E.,, N. O’Connor,, Z. Prágai,, A. C. Ward,, A. Wipat, and, C. R. Harwood. 2005. Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J. Bacteriol. 187: 8063– 8080.
3. Alper,, S., A. Dufour,, D. A. Garsin,, L. Duncan, and, R. Losick. 1996. Role of adenosine nucleotides in the regulation of a stress-response transcription factor in Bacillus subtilis. J. Mol. Biol. 260: 165– 177.
4. Antelmann,, H., S. Engelmann,, R. Schmid,, A. Sorokin,, A. Lapidus, and, M. Hecker. 1997. Expression of a stress- and starvation-induced dps/pexB -homologous gene is controlled by the alternative sigma factor σ B in Bacillus subtilis. J. Bacteriol. 179: 7251– 7256.
5. Aravind, L., and, E. V. Koonin. 2000. The STAS domain—a link between anion transporters and antisigma-factor antagonists. Curr. Biol. 10:R 53– 55.
6. Avila-Pérez,, M.,, J. B. van der Steen,, R. Kort, and, K. J. Hellingwerf. 2010. Red light activates the σ B-mediated stress response of Bacillus subtilis via the energy branch of the upstream signaling cascade. J. Bacteriol. 192: 755– 762.
7. Avila-Pérez,, M., J. Vreede,, Y. Tang,, O. Bende,, A. Losi,, W. Gärtner, and, K. Hellingwerf. 2009. In vivo mutational analysis of YtvA from Bacillus subtilis: mechanism of light activation of the general stress response. J. Biol. Chem. 284: 24958– 24964.
8. Avila-Perez, M.,, K. J. Hellingwerf, and, R. Kort. 2006. Blue light activates the σ B-dependent stress response of Bacillus subtilis via YtvA. J. Bacteriol. 188: 6411– 6414.
9. Beaucher,, J., S. Rodrigue,, P. E. Jacques,, I. Smith,, R. Brzezinski, and, L. Gaudreau. 2002. Novel Mycobacterium tuberculosis anti-s factor antagonists control σ F activity by distinct mechanisms. Mol. Microbiol. 45: 1527– 1540.
10. Begley,, M.,, R. D. Sleator,, C. G. Gahan, and, C. Hill. 2005. Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73: 894– 904.
11. Benson, A. K., and, W. G. Haldenwang. 1992. Characterization of a regulatory network that controls σ B expression in Bacillus subtilis. J. Bacteriol. 174: 749– 757.
12. Benson, A. K., and, W. G. Haldenwang. 1993. Bacillus subtilis σ B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc. Natl. Acad. Sci. USA 90: 2330– 2334.
13. Bernhardt,, J., U. Völker,, A. Völker,, H. Antelmann,, R. Schmid,, H. Mach, and, M. Hecker. 1997. Specific and general stress proteins in Bacillus subtilis—a two-dimensional protein electrophoresis study. Microbiology 143: 999– 1017.
14. Bischoff, M., and, B. Berger-Bächi. 2001. Teicoplanin stress-selected mutations increasing σ B activity in Staphylococcus aureus. Antimicrob. Agents Chemother. 45: 1714– 1720.
15. Bischoff,, M., P. Dunman,, J. Kormanec,, D. Macapagal,, E. Murphy,, W. Mounts,, B. Berger-Bächi, and, S. Projan. 2004. Microarray-based analysis of the Staphylococcus aureus σ B regulon. J. Bacteriol. 186: 4085– 4099.
16. Bork, P.,, N. P. Brown,, H. Hegyi, and, J. Schultz. 1996. The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues. Protein Sci. 5: 1421– 1425.
17. Boylan, S. A.,, A. Rutherford,, S. M. Thomas, and, C. W. Price. 1992. Activation of Bacillus subtilis transcription factor σ B by a regulatory pathway responsive to stationary-phase signals. J. Bacteriol. 174: 3695– 3706.
18. Brigulla,, M., T. Hoffmann,, A. Krisp,, A. Völker,, E. Bremer, and, U. Völker. 2003. Chill induction of the SigB- dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J. Bacteriol. 185: 4305– 4314.
19. Brody, M. S.,, K. Vijay, and, C. W. Price. 2001. Catalytic function of an a/b hydrolase is required for energy stress activation of the σ B transcription factor in Bacillus subtilis. J. Bacteriol. 183: 6422– 6428.
20. Brody, M. S.,, V. Stewart, and, C. W. Price. 2009. Bypass suppression analysis maps the signalling pathway within a multido-main protein: the RsbP energy stress phosphatase 2C from Bacillus subtilis. Mol. Microbiol. 72: 1221– 1234.
21. Bronner,, S., H. Monteil, and, G. Prévost. 2004. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol. Rev. 28: 183– 200.
22. Buttani, V.,, A. Losi,, E. Polverini, and, W. Gärtner. 2006. Blue news: NTP binding properties of the blue-light sensitive YtvA protein from Bacillus subtilis. FEBS Lett. 580: 3818– 3822.
23. Cebrián,, G., N. Sagarzazu,, A. Aertsen,, R. Pagán,, S. Condón, and, P. Mañas. 2009. Role of the alternative sigma factor σ B on Staphylococcus aureus resistance to stresses of relevance to food preservation. J. Appl. Microbiol. 107: 187– 196.
24. Chaturongakul,, S., S. Raengpradub,, M. Wiedmann, and, K. J. Boor. 2008. Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol. 16: 388– 396.
25. Chen, C. C.,, M. D. Yudkin, and, O. Delumeau. 2004. Phosphorylation and RsbX-dependent dephosphorylation of RsbR in the RsbR-RsbS complex of Bacillus subtilis. J. Bacteriol. 186: 6830– 6836.
26. Chen,, C. C.,, R. J. Lewis,, R. Harris,, M. D. Yudkin, and, O. Delumeau. 2003. A supramolecular complex in the environmental stress signalling pathway of Bacillus subtilis. Mol. Microbiol. 49: 1657– 1669.
27. Chen,, P.,, R. E. Ruiz,, Q. Li,, R. F. Silver, and, W. R. Bishai. 2000. Construction and characterization of a Mycobacterium tuberculosis mutant lacking the alternate sigma factor gene, sigF. Infect. Immun. 68: 5575– 5580.
28. Cho,, Y. H.,, E. J. Lee,, B. E. Ahn, and, J. H. Roe. 2001. SigB, an RNA polymerase sigma factor required for osmoprotection and proper differentiation of Streptomyces coelicolor. Mol. Microbiol. 42: 205– 214.
29. de Been,, M.,, M. H. Tempelaars,, W. van Schaik,, R. Moezelaar,, R. J. Siezen, and, T. Abee. 2010. A novel hybrid kinase is essential for regulating the σ B-mediated stress response of Bacillus cereus. Environ. Micriobiol. 12: 730– 745.
30. Delumeau,, O.,, C. C. Chen,, J. W. Murray,, M. D. Yudkin, and, R. J. Lewis. 2006. High-molecular-weight complexes of RsbR and paralogues in the environmental signaling pathway of Bacillus subtilis. J. Bacteriol. 188: 7885– 7892.
31. Delumeau,, O.,, R. J. Lewis, and, M. D. Yudkin. 2002. Protein-protein interactions that regulate the energy stress activation of σ B in Bacillus subtilis. J. Bacteriol. 184: 5583– 5589.
32. Delumeau,, O., S. Dutta,, M. Brigulla,, G. Kuhnke,, S. W. Hardwick,, U. Völker,, M. D. Yudkin, and, R. J. Lewis. 2004. Functional and structural characterization of RsbU, a stress signaling protein phosphatase 2C. J. Biol. Chem. 279: 40927– 40937.
33. DeMaio,, J., Y. Zhang,, C. Ko, and, W. R. Bishai. 1997. Mycobacterium tuberculosis sigF is part of a gene cluster with similarities to the Bacillus subtilis sigF and sigB operons. Tuber. Lung Dis. 78: 3– 12.
34. Derre,, I., G. Rapoport, and, T. Msadek. 1999. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria. Mol. Microbiol. 31: 117– 131.
35. de Vries,, Y. P.,, L. M. Hornstra,, R. D. Atmadja,, W. Schaik,, W. M. de Vos, and, T. Abee. 2005. Deletion of sigB in Bacillus cereus affects spore properties. FEMS Microbiol. Lett. 252: 169– 173.
36. Donegan, N. P., and, A. L. Cheung. 2009. Regulation of the mazEF toxin-antitoxin module in Staphylococcus aureus and its impact on sigB expression. J. Bacteriol. 191: 2795– 2805.
37. Dufour, A., and, W. G. Haldenwang. 1994. Interactions between a Bacillus subtilis anti-s factor (RsbW) and its antagonist (RsbV). J. Bacteriol. 176: 1813– 1820.
38. Duncan, L., and, R. Losick. 1993. SpoIIAB is an anti-s factor that binds to and inhibits transcription by regulatory protein σ F from Bacillus subtilis. Proc. Natl. Acad. Sci. USA 90: 2325– 2329.
39. Engelmann, S., and, M. Hecker. 1996. Impaired oxidative stress resistance of Bacillus subtilis sigB mutants and the role of katA and katE. FEMS Microbiol. Lett. 145: 63– 69.
40. Eymann,, C., D. Becher,, J. Bernhardt,, K. Gronau,, A. Klutzny, and, M. Hecker. 2007. Dynamics of protein phosphorylation on Ser/Thr/Tyr in Bacillus subtilis. Proteomics 7: 3509– 3526.
41. Fernández-Martínez,, L., A. Bishop,, L. Parkes,, R. Del Sol,, P. Salerno,, B. Sevcikova,, V. Mazurakova,, J. Kormanec, and, P. Dyson. 2009. Osmoregulation in Streptomyces coelicolor: modulation of SigB activity by OsaC. Mol. Microbiol. 71: 1250– 1262.
42. Ferreira,, A., D. Sue,, C. P. O’Byrne, and, K. J. Boor. 2003. Role of Listeria monocytogenes σ B in survival of lethal acidic conditions and in the acquired acid tolerance response. Appl. Environ. Microbiol. 69: 2692– 2698.
43. Fouet,, A., O. Namy, and, G. Lambert. 2000. Characterization of the operon encoding the alternative σ B factor from Bacillus anthracis and its role in virulence. J. Bacteriol. 182: 5036– 5045.
44. Fuangthong,, M., S. Atichartpongkul,, S. Mongkolsuk, and, J. D. Helmann. 2001. OhrR is a repressor of ohrA, a key organic hydroperoxide resistance determinant in Bacillus subtilis. J. Bacteriol. 183: 4134– 4141.
45. Gahan, C. G., and, C. Hill. 2005. Gastrointestinal phase of Listeria monocytogenes infection. J. Appl. Microbiol. 98: 1345– 1353.
46. Gaidenko, T. A., and, C. W. Price. 1998. General stress transcription factor σ B and sporulation transcription factor σ H each contribute to survival of Bacillus subtilis under extreme growth conditions. J. Bacteriol. 180: 3730– 3733.
47. Gaidenko,, T. A.,, T. J. Kim,, A. L. Weigel,, M. S. Brody, and, C. W. Price. 2006. The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis. J. Bacteriol. 188: 6387– 6395.
48. Gaidenko, T. A.,, X. Yang,, Y. M. Lee, and, C. W. Price. 1999. Threo-nine phosphorylation of modulator protein RsbR governs its ability to regulate a serine kinase in the environmental stress signaling pathway of Bacillus subtilis. J. Mol. Biol. 288: 29– 39.
49. Garner,, M. R.,, B. L. Njaa,, M. Wiedmann, and, K. J. Boor. 2006. σ B contributes to Listeria monocytogenes gastrointestinal infection but not to systemic spread in the guinea pig infection model. Infect. Immun. 74: 876– 886.
50. Geiman,, D. E.,, D. Kaushal,, C. Ko,, S. Tyagi,, Y. C. Manabe,, B. G. Schroeder,, R. D. Fleischmann,, N. E. Morrison,, P. J. Converse,, P. Chen, and, W. R. Bishai. 2004. Attenuation of late-stage disease in mice infected by the Mycobacterium tuberculosis mutant lacking the SigF alternate sigma factor and identification of SigF-dependent genes by microarray analysis. Infect. Immun. 72: 1733– 1745.
51. Giachino,, P., S. Engelmann, and, M. Bischoff. 2001. σ B activity depends on RsbU in Staphylococcus aureus. J. Bacteriol. 183: 1843– 1852.
52. Glaser,, P., L. Frangeul,, C. Buchrieser,, C. Rusniok,, A. Amend,, F. Baquero,, P. Berche,, H. Bloecker,, P. Brandt,, T. Chakraborty,, A. Charbit,, F. Chetouani,, E. Couvé,, A. de Daruvar,, P. Dehoux,, E. Domann,, G. Domínguez-Bernal,, E. Duchaud,, L. Durant,, O. Dussurget,, K. D. Entian,, H. Fsihi,, F. Garcia-del Portillo,, P. Garrido,, L. Gautier,, W. Goebel,, N. Gómez-López,, T. Hain,, J. Hauf,, D. Jackson,, L. M. Jones,, U. Kaerst,, J. Kreft,, M. Kuhn,, F. Kunst,, G. Kurapkat,, E. Madueño,, A. Maitournam,, J. M. Vicente,, E. Ng,, H. Nedjari,, G. Nordsiek,, S. Novella,, B. de Pablos,, J. C. Pérez-Diaz,, R. Purcell,, B. Remmel,, M. Rose,, T. Schlueter,, N. Simoes,, A. Tierrez,, J. A. Vázquez-Boland,, H. Voss,, J. Wehland, and, P. Cossart. 2001. Comparative genomics of Listeria species. Science 294: 849– 852.
53. Gohar,, M., K. Faegri,, S. Perchat,, S. Ravnum,, O. A. Økstad,, M. Gominet,, A. B. Kolstø, and, D. Lereclus. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS One 3: e2793.
54. Gray, M. J.,, N. E. Freitag, and, K. J. Boor. 2006. How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect. Immun. 74: 2505– 2512.
55. Greenstein,, A. E.,, J. A. MacGurn,, C. E. Baer,, A. M. Falick,, J. S. Cox, and, T. Alber. 2007. M. tuberculosis Ser/Thr protein kinase D phosphorylates an anti-anti-sigma factor homolog. PLoS Pathog. 3: e49.
56. Greenstein, A. E.,, M. Hammel,, A. Cavazos, and, T. Alber. 2009. Interdomain communication in the Mycobacterium tuberculosis environmental phosphatase Rv1364c. J. Biol. Chem. 284: 29828– 29835.
57. Hain,, T., H. Hossain,, S. S. Chatterjee,, S. Machata,, U. Volk,, S. Wagner,, B. Brors,, S. Haas,, C. T. Kuenne,, A. Billion,, S. Otten,, J. Pané-Farré,, S. Engelmann, and, T. Chakraborty. 2008. Temporal transcriptomic analysis of the Listeria monocyto-genes EGD-e σ B regulon. BMC Microbiol. 8: 20.
58. Haldenwang, W. G., and, R. Losick. 1979. A modified RNA polymerase transcribes a cloned gene under sporulation control in Bacillus subtilis. Nature 282: 256– 260.
59. Haldenwang, W. G., and, R. Losick. 1980. Novel RNA polymerase sigma factor from Bacillus subtilis. Proc. Natl. Acad. Sci. USA 77: 7000– 7004.
60. Hardwick,, S. W.,, J. Pané-Farré,, O. Delumeau,, J. Marles-Wright,, J. W. Murray,, M. Hecker, and, R. J. Lewis. 2007. Structural and functional characterization of partner switching regulating the environmental stress response in Bacillus subtilis. J. Biol. Chem. 282: 11562– 11572.
61. Hecker, M.,, A. Reder,, S. Fuchs,, M. Pagels, and, S. Engelmann. 2009. Physiological proteomics and stress/starvation responses in Bacillus subtilis and Staphylococcus aureus. Res. Microbiol. 160: 245– 258.
62. Hecker,, M., J. Pané-Farré, and, U. Völker. 2007. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 61: 215– 236.
63. Hecker, M., and, U. Völker. 2001. General stress response of Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44: 35– 91.
64. Helmann,, J. D.,, M. F. Wu,, A. Gaballa,, P. A. Kobel,, M. M. Morshedi,, P. Fawcett, and, C. Paddon. 2003. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J. Bacteriol. 185: 243– 253.
65. Helmann,, J. D.,, M. F. Wu,, P. A. Kobel,, F. J. Gamo,, M. Wilson,, M. M. Morshedi,, M. Navre, and, C. Paddon. 2001. Global transcriptional response of Bacillus subtilis to heat shock. J. Bacteriol. 183: 7318– 7328.
66. Höper,, D., J. Bernhardt, and, M. Hecker. 2006. Salt stress adaptation of Bacillus subtilis: a physiological proteomics approach. Proteomics 6: 1550– 1562.
67. Höper,, D., U. Völker, and, M. Hecker. 2005. Comprehensive characterization of the contribution of individual SigB-dependent general stress genes to stress resistance of Bacillus subtilis. J. Bacteriol. 187: 2810– 2826.
68. Hua, L. 2004. Partner switching signaling mechanism in bacteria. Ph.D. thesis, University of California, Davis.
69. Hua,, L.,, P. S. Hefty,, Y. J. Lee,, Y. M. Lee,, R. S. Stephens, and, C. W. Price. 2006. Core of the partner switching signalling mechanism is conserved in the obligate intracellular pathogen Chlamydia trachomatis. Mol. Microbiol. 59: 623– 636.
70. Igoshin,, O. A.,, M. S. Brody,, C. W. Price, and, M. A. Savageau. 2007. Distinctive topologies of partner-switching signaling networks correlate with their physiological roles. J. Mol. Biol. 369: 1333– 1352.
71. Jonsson, I. M.,, S. Arvidson,, S. Foster, and, A. Tarkowski. 2004. Sigma factor B and RsbU are required for virulence in Staphylococcus aureus-induced arthritis and sepsis. Infect. Immun. 72: 6106– 6111.
72. Kaneko,, T., N. Tanaka, and, T. Kumasaka. 2005. Crystal structures of RsbQ, a stress-response regulator in Bacillus subtilis. Protein Sci. 14: 558– 565.
73. Kang,, C. M.,, M. S. Brody,, S. Akbar,, X. Yang, and, C. W. Price. 1996. Homologous pairs of regulatory proteins control activity of Bacillus subtilis transcription factor σ B in response to environmental stress. J. Bacteriol. 178: 3846– 3853.
74. Karls,, R. K.,, J. Guarner,, D. N. McMurray,, K. A. Birkness, and, F. D. Quinn. 2006. Examination of Mycobacterium tuberculosis sigma factor mutants using low-dose aerosol infection of guinea pigs suggests a role for SigC in pathogenesis. Microbiology 152: 1591– 1600.
75. Kazmierczak,, M. J.,, S. C. Mithoe,, K. J. Boor, and, M. Wiedmann. 2003. Listeria monocytogenes σ B regulates stress response and virulence functions. J. Bacteriol. 185: 5722– 5734.
76. Kim, T. J.,, T. A. Gaidenko, and, C. W. Price. 2004a. A multicomponent protein complex mediates environmental stress signaling in Bacillus subtilis. J. Mol. Biol. 341: 135– 150.
77. Kim, T. J.,, T. A. Gaidenko, and, C. W. Price. 2004b. In vivo phosphorylation of partner switching regulators correlates with stress transmission in the environmental signaling pathway of Bacillus subtilis. J. Bacteriol. 186: 6124– 6132.
78. Koburger, T.,, J. Weibezahn,, J. Bernhardt,, G. Homuth, and, M. Hecker. 2005. Genome-wide mRNA profiling in glucose starved Bacillus subtilis cells. Mol. Genet. Genomics 274: 1– 12.
79. Koonin,, E. V.,, L. Aravind, and, M. Y. Galperin. 2000. A comparative-genomic view of the microbial stress response, P. 417–444. In G. Storz and, R. Hengge-Aronis (ed.), Bacterial Stress Responses. ASM Press, Washington, DC.
80. Kozak,, N. A.,, S. Mattoo,, A. K. Foreman-Wykert,, J. P. Whitelegge, and, J. F. Miller. 2005. Interactions between partner switcher orthologs BtrW and BtrV regulate type III secretion in Bordetella. J. Bacteriol. 187: 5665– 5676.
81. Krüger, E., and, M. Hecker. 1998. The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J. Bacteriol. 180: 6681– 6688.
82. Kuo, S., B. Demeler, and, W. G. Haldenwang. 2008. The growth-promoting and stress response activities of the Bacillus subtilis GTP binding protein Obg are separable by mutation. J. Bacteriol. 190: 6625– 6635.
83. Lauderdale,, K. J.,, B. R. Boles,, A. L. Cheung, and, A. R. Horswill. 2009. Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect. Immun. 77: 1623– 1635.
84. Lee,, E. J.,, N. Karoonuthaisiri,, H. S. Kim,, J. H. Park,, C. J. Cha,, C. M. Kao, and, J. H. Roe. 2005. A master regulator σ B governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor. Mol. Microbiol. 57: 1252– 1264.
85. Lee,, E. J.,, Y. H. Cho,, H. S. Kim,, B. E. Ahn, and, J. H. Roe. 2004. Regulation of σ B by an anti- and an anti-anti-sigma factor in Streptomyces coelicolor in response to osmotic stress. J. Bacteriol. 186: 8490– 8498.
86. Losi, A.,, E. Polverini,, B. Quest, and, W. Gärtner. 2002. First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys. J. 82: 2627– 2634.
87. Manganelli,, R., R. Provvedi,, S. Rodrigue,, J. Beaucher,, L. Gaudreau, and, I. Smith. 2004. s factors and global gene regulation in Mycobacterium tuberculosis. J. Bacteriol. 186: 895– 902.
88. Marles-Wright,, J., T. Grant,, O. Delumeau,, G. van Duinen,, S. J. Firbank,, P. J. Lewis,, J. W. Murray,, J. A. Newman,, M. B. Quin,, P. R. Race,, A. Rohou,, W. Tichelaar,, M. van Heel, and, R. J. Lewis. 2008. Molecular architecture of the “stressosome,” a signal integration and transduction hub. Science 322: 92– 96.
89. Mascher,, T.,, N. G. Margulis,, T. Wang,, R. W. Ye, and, J. D. Helmann. 2003. Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol. Microbiol. 50: 1591– 1604.
90. Mattoo,, S.,, M. H. Yuk,, L. L. Huang, and, J. F. Miller. 2004. Regulation of type III secretion in Bordetella. Mol. Microbiol. 52: 1201– 1214.
91. Milohanic,, E., P. Glaser,, J. Y. Coppée,, L. Frangeul,, Y. Vega,, J. A. Vázquez-Boland,, F. Kunst,, P. Cossart, and, C. Buchrieser. 2003. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol. 47: 1613– 1625.
92. Min,, K. T.,, C. M. Hilditch,, B. Diederich,, J. Errington, and, M. D. Yudkin. 1993. σ F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-s factor that is also a protein kinase. Cell 74: 735– 742.
93. Mittenhuber, G. 2002. A phylogenomic study of the general stress response sigma factor σ B of Bacillus subtilis and its regulatory proteins. J. Mol. Microbiol. Biotechnol. 4: 427– 452.
94. Möglich, A., and, K. Moffat. 2007. Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J. Mol. Biol. 373: 112– 126.
95. Möglich, A.,, R. A. Ayers, and, K. Moffat. 2009. Design and signaling mechanism of light-regulated histidine kinases. J. Mol. Biol. 385: 1433– 1444.
96. Moore,, C. M.,, M. M. Nakano,, T. Wang,, R. W. Ye, and, J. D. Helmann. 2004. Response of Bacillus subtilis to nitric oxide and the nitrosating agent sodium nitroprusside. J. Bacteriol. 186: 4655– 4664.
97. Murray, J. W.,, O. Delumeau, and, R. J. Lewis. 2005. Structure of a nonheme globin in environmental stress signaling. Proc. Natl. Acad. Sci. USA 102: 17320– 17325.
98. Nakano, M. M.,, H. Geng,, S. Nakano, and, K. Kobayashi. 2006. The nitric oxide-responsive regulator NsrR controls ResDE-dependent gene expression. J. Bacteriol. 188: 5878– 5887.
99. Novick, R. P., and, E. Geisinger. 2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42: 541– 564.
100. Ollinger,, J., B. Bowen,, M. Wiedmann,, K. J. Boor, and, T. M. Bergholz. 2009. Listeria monocytogenes σ B modulates PrfA-mediated virulence factor expression. Infect. Immun. 77: 2113– 2124.
101. Pané-Farré, J.,, B. Jonas,, K. Förstner,, S. Engelmann, and, M. Hecker. 2006. The σ B regulon in Staphylococcus aureus and its regulation. Int. J. Med. Microbiol. 296: 237– 258.
102. Pané-Farré,, J., B. Jonas,, S. W. Hardwick,, K. Gronau,, R. J. Lewis,, M. Hecker, and, S. Engelmann. 2009. Role of RsbU in controlling SigB activity in Staphylococcus aureus following alkaline stress. J. Bacteriol. 191: 2561– 2573.
103. Pané-Farré, J.,, R. J. Lewis, and, J. Stülke. 2005. The RsbRST stress module in bacteria: a signalling system that may interact with different output modules. J Mol. Microbiol. Biotechnol 9: 65– 76.
104. Petersohn,, A., M. Brigulla,, S. Haas,, J. D. Hoheisel,, U. Völker, and, M. Hecker. 2001. Global analysis of the general stress response of Bacillus subtilis. J. Bacteriol. 183: 5617– 5631.
105. Price, C. W. 2000. Protective function and regulation of the general stress response in Bacillus subtilis and related gram-positive bacteria, P. 179–197. In G. Storz and, R. Hengge-Aronis (ed.), Bacterial Stress Responses. ASM Press, Washington, DC.
106. Price,, C. W. 2002. General stress response, P. 369–384. In A. L. Sonenshein,, J. A. Hoch, and, R. Losick (ed.), Bacillus subtilis and Its Closest Relatives. ASM Press, Washington, DC.
107. Price,, C. W.,, P. Fawcett,, H. Ceremonie,, N. Su,, C. K. Murphy, and, P. Youngman. 2001. Genome-wide analysis of the general stress response in Bacillus subtilis. Mol. Microbiol. 41: 757– 774.
108. Rauch, M.,, Q. Luo,, S. Müller-Altrock, and, W. Goebel. 2005. SigB-dependent in vitro transcription of prfA and some newly identified genes of Listeria monocytogenes whose expression is affected by PrfA in vivo. J. Bacteriol. 187: 800– 804.
109. Reder,, A., D. Höper,, C. Weinberg,, U. Gerth,, M. Fraunholz, and, M. Hecker. 2008. The Spx paralogue MgsR (YqgZ) controls a subregulon within the general stress response of Bacillus subtilis. Mol. Microbiol. 69: 1104– 1120.
110. Reeves,, A., U. Gerth,, U. Völker, and, W. G. Haldenwang. 2007. ClpP modulates the activity of the Bacillus subtilis stress response transcription factor, σ B. J. Bacteriol. 189: 6168– 6175.
111. Reeves, A., and, W. G. Haldenwang. 2007. Isolation and characterization of dominant mutations in the Bacillus subtilis stressosome components RsbR and RsbS. J. Bacteriol. 189: 1531– 1541.
112. Schwab,, U., B. Bowen,, C. Nadon,, M. Wiedmann, and, K. J. Boor. 2005. The Listeria monocytogenes prfA P2 promoter is regulated by sigma B in a growth phase dependent manner. FEMS Microbiol. Lett. 245: 329– 336.
113. Scortti,, M.,, H. J. Monzó,, L. Lacharme-Lora,, D. A. Lewis, and, J. A. Vázquez-Boland. 2007. The PrfA virulence regulon. Microbes Infect. 9: 1196– 1207.
114. Scott, J. M.,, N. Smirnova, and, W. G. Haldenwang. 1999. A Bacillus-specific factor is needed to trigger the stress-activated phosphatase/kinase cascade of σ B induction. Biochem. Biophys. Res. Commun. 257: 106– 110.
115. Scott, J. M., and, W. G. Haldenwang. 1999. Obg, an essential GTP binding protein of Bacillus subtilis, is necessary for stress activation of transcription factor σ B. J. Bacteriol. 181: 4653– 4660.
116. Senn,, M. M.,, P. Giachino,, D. Homerova,, A. Steinhuber,, J. Strassner,, J. Kormanec,, U. Flückiger,, B. Berger-Bächi, and, M. Bischoff. 2005. Molecular analysis and organization of the σ B operon in Staphylococcus aureus. J. Bacteriol. 187: 8006– 8019.
117. Shi,, L.,, K. M. Bischoff, and, P. J. Kennelly. 1999. The icfG gene cluster of Synechocystis sp. strain PCC 6803 encodes an Rsb/ Spo-like protein kinase, protein phosphatase, and two phosphoproteins. J. Bacteriol. 181: 4761– 4767.
118. Shin, J. H.,, M. S. Brody, and, C. W. Price. 2010. Physical and antibiotic stresses require activation of the RsbU phosphatase to induce the general stress response in Listeria monocytogenes. Microbiology 156: 2660– 2669.
119. Sleator, R. D.,, D. Watson,, C. Hill, and, C. G. Gahan. 2009. The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology 155: 2463– 2475.
120. Tam,, L. T.,, H. Antelmann,, C. Eymann,, D. Albrecht,, J. Bernhardt, and, M. Hecker. 2006. Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2-D gel image color coding approach. Proteomics 6: 4565– 4585.
121. Taylor, B. L., and, I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63: 479– 506.
122. Toledo-Arana,, A., O. Dussurget,, G. Nikitas,, N. Sesto,, H. GuetRevillet,, D. Balestrino,, E. Loh,, J. Gripenland,, T. Tiensuu,, K. Vaitkevicius,, M. Barthelemy,, M. Vergassola,, M. A. Nahori,, G. Soubigou,, B. Régnault,, J. Y. Coppée,, M. Lecuit,, J. Johansson, and, P. Cossart. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950– 956.
123. van Schaik,, W.,, M. H. Tempelaars,, J. A. Wouters,, W. M. de Vos, and, T. Abee. 2004. The alternative sigma factor σ B of Bacillus cereus: response to stress and role in heat adaptation. J. Bacteriol. 186: 316– 325.
124. van Schaik,, W.,, M. H. Tempelaars,, M. H. Zwietering,, W. M. de Vos, and, T. Abee. 2005. Analysis of the role of RsbV, RsbW, and RsbY in regulating σ B activity in Bacillus cereus. J. Bacteriol. 187: 5846– 5851.
125. van Schaik,, W., M. van der Voort,, D. Molenaar,, R. Moezelaar,, W. M. de Vos, and, T. Abee. 2007. Identification of the σ B regulon of Bacillus cereus and conservation of σ B-regulated genes in low-GC-content gram-positive bacteria. J. Bacteriol. 189: 4384– 4390.
126. Vijay,, K.,, M. S. Brody,, E. Fredlund, and, C. W. Price. 2000. A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the σ B transcription factor of Bacillus subtilis. Mol. Microbiol. 35: 180– 188.
127. Viollier,, P. H.,, G. H. Kelemen,, G. E. Dale,, K. T. Nguyen,, M. J. Buttner, and, C. J. Thompson. 2003. Specialized osmotic stress response systems involve multiple SigB-like sigma factors in Streptomyces coelicolor. Mol. Microbiol. 47: 699– 714.
128. Voelker,, U., A. Voelker,, B. Maul,, M. Hecker,, A. Dufour, and, W. G. Haldenwang. 1995. Separate mechanisms activate σ B of Bacillus subtilis in response to environmental and metabolic stresses. J. Bacteriol. 177: 3771– 3780.
129. Voelker, U., A. Voelker, and, W. G. Haldenwang. 1996. Reactivation of the Bacillus subtilis anti-σ B antagonist, RsbV, by stress- or starvation-induced phosphatase activities. J. Bacteriol. 178: 5456– 5463.
130. Voelker, U.,, T. Luo,, N. Smirnova, and, W. Haldenwang. 1997. Stress activation of Bacillus subtilis σ B can occur in the absence of the σ B negative regulator RsbX. J. Bacteriol. 179: 1980– 1984.
131. Völker,, U., B. Maul, and, M. Hecker. 1999. Expression of the σ B-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. J. Bacteriol. 181: 3942– 3948.
132. Wang,, S. W.,, C. Y. Chen,, J. T. Tseng,, S. H. Liang,, S. C. Chen,, C. Hsieh,, Y. H. Chen, and, C. C. Chen. 2009. orf4 of the Bacillus cereus sigB gene cluster encodes a general stress-inducible Dps-like bacterioferritin. J. Bacteriol. 191: 4522– 4533.
133. Williams,, E. P.,, J. H. Lee,, W. R. Bishai,, C. Colantuoni, and, P. C. Karakousis. 2007. Mycobacterium tuberculosis SigF regulates genes encoding cell wall-associated proteins and directly regulates the transcriptional regulatory gene phoY1. J. Bacteriol. 189: 4234– 4242.
134. Wu,, S., H. de Lencastre, and, A. Tomasz. 1996. Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing. J. Bacteriol. 178: 6036– 6042.
135. Yang,, X.,, C. M. Kang,, M. S. Brody, and, C. W. Price. 1996. Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev. 10: 2265– 2275.
136. Zhang, S., and, W. G. Haldenwang. 2005. Contributions of ATP, GTP, and redox state to nutritional stress activation of the Bacillus subtilis σ B transcription factor. J. Bacteriol. 187: 7554– 7560.
137. Ziebandt,, A. K.,, D. Becher,, K. Ohlsen,, J. Hacker,, M. Hecker, and, S. Engelmann. 2004. The influence of agr and σ B in growth phase dependent regulation of virulence factors in Staphylococcus aureus. Proteomics 4: 3034– 3047.
138. Zuber, P. 2009. Management of oxidative stress in Bacillus. Annu. Rev. Microbiol. 63: 575– 597.

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