The Bacillus subtilis σM regulon and its contribution to cell envelope stress responses

Molecular Microbiology

Volumn 67, Issue 4, 2008, Pages 830-848

  Eiamphungporn, Warawan ^a   Helmann, John D ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; SIGMA FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SPX; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL MEMBRANE; CELL DIVISION; CELL STRESS; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REGULON; TRANSCRIPTION REGULATION;

5' UNTRANSLATED REGIONS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; CELL MEMBRANE; CELL WALL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OPERON; REGULON; SIGMA FACTOR;

BACILLUS SUBTILIS;

EID: 38449121941     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06090.x     Document Type: Article

References (94)

1. E-dependent envelope stress response. Mol Microbiol 52 : 613 619.
2. Antelmann, H., Scharf, C. Hecker, M. (2000) Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J Bacteriol 182 : 4478 4490.
3. Asai, K., Yamaguchi, H., Kang, C.M., Yoshida, K., Fujita, Y. Sadaie, Y. (2003) DNA microarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett 220 : 155 160.
4. Bauer, R. Dicks, L.M. (2005) Mode of action of lipid II-targeting lantibiotics. Int J Food Microbiol 101 : 201 216.
5. Bejerano-Sagie, M., Oppenheimer-Shaanan, Y., Berlatzky, I., Rouvinski, A., Meyerovich, M. Ben-Yehuda, S. (2006) A checkpoint protein that scans the chromosome for damage at the start of sporulation in Bacillus subtilis. Cell 125 : 679 690.
6. Bernard, R., El Ghachi, M., Mengin-Lecreulx, D., Chippaux, M. Denizot, F. (2005) BcrC from Bacillus subtilis acts as an undecaprenyl pyrophosphate phosphatase in bacitracin resistance. J Biol Chem 280 : 28852 28857.
7. Bhavsar, A.P. Brown, E.D. (2006) Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol Microbiol 60 : 1077 1090.
8. Bisicchia, P., Noone, D., Lioliou, E., Howell, A., Quigley, S., Jensen, T., et al. (2007) The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol Microbiol 65 : 180 200.
9. Bolhuis, A., Broekhuizen, C.P., Sorokin, A., van Roosmalen, M.L., Venema, G., Bron, S., et al. (1998) SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins. J Biol Chem 273 : 21217 21224.
10. Borukhov, S., Lee, J. Laptenko, O. (2005) Bacterial transcription elongation factors: new insights into molecular mechanism of action. Mol Microbiol 55 : 1315 1324.
11. Breukink, E. de Kruijff, B. (2006) Lipid II as a target for antibiotics. Nat Rev Drug Discov 5 : 321 332.
12. Britton, R.A., Kuster-Schock, E., Auchtung, T.A. Grossman, A.D. (2007) SOS induction in a subpopulation of structural maintenance of chromosome (Smc) mutant cells in Bacillus subtilis. J Bacteriol 189 : 4359 4366.
13. Butcher, B.G. Helmann, J.D. (2006) Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol Microbiol 60 : 765 782.
14. Cao, M. Helmann, J.D. (2002) Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors. J Bacteriol 184 : 6123 6129.
15. X factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J Bacteriol 186 : 1136 1146.
16. W, an extracytoplasmic-function σ factor in Bacillus subtilis. J Bacteriol 183 : 2380 2383.
17. 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.
18. M regulons. Mol Microbiol 45 : 1267 1276.
19. Y and its target promoters. J Bacteriol 185 : 4883 4890.
20. M, an extracytoplasmic function σ factor, and is conferred by YqjL and BcrC. J Bacteriol 187 : 2948 2956.
21. Crouvoisier, M., Auger, G., Blanot, D. Mengin-Lecreulx, D. (2007) Role of the amino acid invariants in the active site of MurG as evaluated by site-directed mutagenesis. Biochimie.
22. Daniel, R.A. Errington, J. (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113 : 767 776.
23. Darwin, A.J. (2005) The phage-shock-protein response. Mol Microbiol 57 : 621 628.
24. Duque, E., Rodriguez-Herva, J.J., de la Torre, J., Dominguez-Cuevas, P., Munoz-Rojas, J. Ramos, J.L. (2007) The RpoT regulon of Pseudomonas putida DOT-T1E and its role in stress endurance against solvents. J Bacteriol 189 : 207 219.
25. Eisen, M.B., Spellman, P.T., Brown, P.O. Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95 : 14863 14868.
26. Errington, J., Daniel, R.A. Scheffers, D.J. (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67 : 52 65, Table of contents.
27. Foster, S.J. Popham, D.L. (2002) Structure and synthesis of cell wall, spore cortex, teichoic acids, S-layers, and capsules. In Bacillus Subtilis and its Closest Relatives: From Genes to Cells. Sonenshein, A.L., Hoch, J. Losick, R. (eds). Washington, DC : ASM Press, pp. 21 41.
28. Grundling, A. Schneewind, O. (2007) Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc Natl Acad Sci USA 104 : 8478 8483.
29. Gustafsson, M.C., Palmer, C.N., Wolf, C.R. von Wachenfeldt, C. (2001) Fatty-acid-displaced transcriptional repressor, a conserved regulator of cytochrome P450 102 transcription in Bacillus species. Arch Microbiol 176 : 459 464.
30. Gustafsson, M.C., Roitel, O., Marshall, K.R., Noble, M.A., Chapman, S.K., Pessegueiro, A., et al. (2004) Expression, purification, and characterization of Bacillus subtilis cytochromes P450 CYP102A2 and CYP102A3: flavocytochrome homologues of P450 BM3 from Bacillus megaterium. Biochemistry 43 : 5474 5487.
31. Harry, E.J., Rowland, S.L., Malo, M.S. Wake, R.G. (1994) Expression of divIB of Bacillus subtilis during vegetative growth. J Bacteriol 176 : 1172 1179.
32. Helmann, J.D. (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46 : 47 110.
33. W protein and intrinsic resistance to antimicrobial compounds. Sci Prog 89 : 243 266.
34. Henriques, A.O., Glaser, P., Piggot, P.J. Moran, C.P., Jr (1998) Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol 28 : 235 247.
35. de Hoon, M.J., Imoto, S., Nolan, J. Miyano, S. (2004) Open source clustering software. Bioinformatics 20 : 1453 1454.
36. 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.
37. X factor using a consensus-directed search. J Mol Biol 279 : 165 173.
38. X regulon. J Bacteriol 180 : 3765 3770.
39. W. Mol Microbiol 31 : 361 371.
40. Hunt, A., Rawlins, J.P., Thomaides, H.B. Errington, J. (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152 : 2895 2907.
41. Hutter, B., Schaab, C., Albrecht, S., Borgmann, M., Brunner, N.A., Freiberg, C., et al. (2004a) Prediction of mechanisms of action of antibacterial compounds by gene expression profiling. Antimicrob Agents Chemother 48 : 2838 2844.
42. Hutter, B., Fischer, C., Jacobi, A., Schaab, C. Loferer, H. (2004b) Panel of Bacillus subtilis reporter strains indicative of various modes of action. Antimicrob Agents Chemother 48 : 2588 2594.
43. Hyyrylainen, H.L., Sarvas, M. Kontinen, V.P. (2005) Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl Microbiol Biotechnol 67 : 389 396.
44. Ikeuchi, Y., Soma, A., Ote, T., Kato, J., Sekine, Y. Suzuki, T. (2005) molecular mechanism of lysidine synthesis that determines tRNA identity and codon recognition. Mol Cell 19 : 235 246.
45. Jervis, A.J., Thackray, P.D., Houston, C.W., Horsburgh, M.J. Moir, A. (2007) SigM-responsive genes of Bacillus subtilis and their promoters. J Bacteriol 189 : 4534 4538.
46. Jordan, S., Junker, A., Helmann, J.D. Mascher, T. (2006) Regulation of LiaRS-dependent gene expression in Bacillus subtilis: identification of inhibitor proteins, regulator binding sites, and target genes of a conserved cell envelope stress-sensing two-component system. J Bacteriol 188 : 5153 5166.
47. Kohanski, M.A., Dwyer, D.J., Hayete, B., Lawrence, C.A. Collins, J.J. (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130 : 797 810.
48. Lee, T.R., Hsu, H.P. Shaw, G.C. (2001) Transcriptional regulation of the Bacillus subtilis bscR-CYP102A3 operon by the BscR repressor and differential induction of cytochrome CYP102A3 expression by oleic acid and palmitate. J Biochem (Tokyo) 130 : 569 574.
49. Leelakriangsak, M. Zuber, P. (2007) Transcription from the P3 promoter of the Bacillus subtilis spx gene is induced in response to disulfide stress. J Bacteriol 189 : 1727 1735.
50. Leelakriangsak, M., Kobayashi, K. Zuber, P. (2007) Dual negative control of spx transcription initiation from the P3 promoter by repressors PerR and YodB in Bacillus subtilis. J Bacteriol 189 : 1736 1744.
51. Lombardo, M.J. Rosenberg, S.M. (2000) radC102 of Escherichia coli is an allele of. Recg J Bacteriol 182 : 6287 6291.
52. Lovett, S.T. (2006) Replication arrest-stimulated recombination: dependence on the RecA paralog, RadA/Sms and translesion polymerase, DinB. DNA Repair (Amst) 5 : 1421 1427.
53. Martinez, B., Zomer, A.L., Rodriguez, A., Kok, J. Kuipers, O.P. (2007) Cell envelope stress induced by the bacteriocin Lcn972 is sensed by the Lactococcal two-component system CesSR. Mol Microbiol 64 : 473 486.
54. 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.
55. Mascher, T., Zimmer, S.L., Smith, T.A. Helmann, J.D. (2004) Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob Agents Chemother 48 : 2888 2896.
56. Mascher, T., Helmann, J.D. Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70 : 910 938.
57. Mascher, T., Hachmann, A.B. Helmann, J.D. (2007) Regulatory overlap and functional redundancy among Bacillus subtilis extracytoplasmic function sigma factors. J Bacteriol 189 : 6919 6927.
58. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Habor, NY : Cold Spring Harbor Laboratory, pp. 352 355.
59. M, two σ factors of the extracytoplasmic function subfamily, are required for septum and wall synthesis under batch culture conditions. Mol Microbiol 49 : 1435 1447.
60. Nakano, S., Kuster-Schock, E., Grossman, A.D. Zuber, P. (2003a) Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc Natl Acad Sci USA 100 : 13603 13608.
61. Nakano, S., Nakano, M.M., Zhang, Y., Leelakriangsak, M. Zuber, P. (2003b) A regulatory protein that interferes with activator-stimulated transcription in bacteria. Proc Natl Acad Sci USA 100 : 4233 4238.
62. Nakano, S., Erwin, K.N., Ralle, M. Zuber, P. (2005) Redox-sensitive transcriptional control by a thiol/disulphide switch in the global regulator, Spx. Mol Microbiol 55 : 498 510.
63. Nanamiya, H., Kasai, K., Nozawa, A., Yun, C.-S., Narisawa, T., Murakami, K., et al. (2007) Identification and functional analysis of novel (p) ppGpp synthetase genes in Bacillus subtilis. Mol Microbiology 67 : 291 304.
64. Ogura, M. Fujita, Y. (2007) Bacillus subtilis rapD, a direct target of transcription repression by RghR, negatively regulates srfA expression. FEMS Microbiol Lett 268 : 73 80.
65. Ohki, R., Tateno, K., Okada, Y., Okajima, H., Asai, K., Sadaie, Y., et al. (2003a) A bacitracin-resistant Bacillus subtilis gene encodes a homologue of the membrane-spanning subunit of the Bacillus licheniformis ABC transporter. J Bacteriol 185 : 51 59.
66. Ohki, R., Giyanto, Tateno, K., Masuyama, W., Moriya, S., Kobayashi, K. Ogasawara, N. (2003b) The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol Microbiol 49 : 1135 1144.
67. Ollinger, J., Song, K.B., Antelmann, H., Hecker, M. Helmann, J.D. (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188 : 3664 3673.
68. R regulon. Mol Microbiol 42 : 1007 1020.
69. Pedersen, L.B. Setlow, P. (2000) Penicillin-binding protein-related factor A is required for proper chromosome segregation in Bacillus subtilis. J Bacteriol 182 : 1650 1658.
70. B-dependent genes in Bacillus subtilis using a promoter consensus-directed search and oligonucleotide hybridization. J Bacteriol 181 : 5718 5724.
71. Pietiainen, M., Gardemeister, M., Mecklin, M., Leskela, S., Sarvas, M. Kontinen, V.P. (2005) Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type σfactors and two-component signal transduction systems. Microbiology 151 : 1577 1592.
72. Price, C.W., Fawcett, P., Ceremonie, 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.
73. W. J Bacteriol 183 : 1921 1927.
74. Raivio, T.L. (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56 : 1119 1128.
75. Raivio, T.L. Silhavy, T.J. (2001) Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55 : 591 624.
76. Real, G. Henriques, A.O. (2006) Localization of the Bacillus subtilis murB gene within the dcw cluster is important for growth and sporulation. J Bacteriol 188 : 1721 1732.
77. E stress response in related genomes. PLoS Biol 4 : e2.
78. Rowley, G., Spector, M., Kormanec, J. Roberts, M. (2006) Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat Rev Microbiol 4 : 383 394.
79. Salzberg, L.I. Helmann, J.D. (2007) An antibiotic-inducible cell wall-associated protein that protects Bacillus subtilis from autolysis. J Bacteriol 189 : 4671 4680.
80. Sanchez, H., Kidane, D., Reed, P., Curtis, F.A., Cozar, M.C., Graumann, P.L., et al. (2005) The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilis. Genetics 171 : 873 883.
81. Sierro, N., Makita, Y., de Hoon, M. Nakai, K. (2007) DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res (in press). doi:10.1093/nar/gkm910
82. Slack, F.J., Mueller, J.P., Strauch, M.A., Mathiopoulos, C. Sonenshein, A.L. (1991) Transcriptional regulation of a Bacillus subtilis dipeptide transport operon. Mol Microbiol 5 : 1915 1925.
83. Stewart, G.C. (2005) Taking shape: control of bacterial cell wall biosynthesis. Mol Microbiol 57 : 1177 1181.
84. Strauch, M.A., Bobay, B.G., Cavanagh, J., Yao, F., Wilson, A. Le Breton, Y. (2007) Abh and AbrB control of Bacillus subtilis antimicrobial gene expression. J Bacteriol 189 : 7720 7732.
85. Tamehiro, N., Okamoto-Hosoya, Y., Okamoto, S., Ubukata, M., Hamada, M., Naganawa, H. Ochi, K. (2002) Bacilysocin, a novel phospholipid antibiotic produced by Bacillus subtilis 168. Antimicrob Agents Chemother 46 : 315 320.
86. M, 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.
87. Tojo, S., Matsunaga, M., Matsumoto, T., Kang, C.M., Yamaguchi, H., Asai, K., et al. (2003) Organization and expression of the Bacillus subtilis sigY operon. J Biochem (Tokyo) 134 : 935 946.
88. Urban, A., Eckermann, S., Fast, B., Metzger, S., Gehling, M., Ziegelbauer, K., et al. (2007) Novel whole-cell antibiotic biosensors for compound discovery. Appl Environ Microbiol 73 : 6436 6443.
89. Veiga, P., Bulbarela-Sampieri, C., Furlan, S., Maisons, A., Chapot-Chartier, M.P., Erkelenz, M., et al. (2007) SpxB regulates O-acetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J Biol Chem 282 : 19342 19354.
90. Wecke, T., Veith, B., Ehrenreich, A. Mascher, T. (2006) Cell envelope stress response in Bacillus licheniformis: integrating comparative genomics, transcriptional profiling, and regulon mining to decipher a complex regulatory network. J Bacteriol 188 : 7500 7511.
91. W regulon. Mol Microbiol 41 : 59 71.
92. V-dependent genes of Bacillus subtilis. FEMS Microbiol Lett 253 : 221 229.
93. Zheng, J., Singh, V.K. Jia, Z. (2005) Identification of an ITPase/XTPase in Escherichia coli by structural and biochemical analysis. Structure 13 : 1511 1520.
94. Zuber, P. (2004) Spx-RNA polymerase interaction and global transcriptional control during oxidative stress. J Bacteriol 186 : 1911 1918.