The SigF regulon in Mycobacterium smegmatis reveals roles in adaptation to stationary phase, heat, and oxidative stress

Journal of Bacteriology

Volumn 192, Issue 10, 2010, Pages 2491-2502

  Hümpel, Anja ^a   Gebhard, Susanne ^a,b   Cook, Gregory M ^a   Berney, Michael ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; HEME; MANGANESE; PHOP PROTEIN; REGULATOR PROTEIN; SIGMA FACTOR; SIGMA FACTOR H3; SIGMA FACTOR REGULON; SUPEROXIDE DISMUTASE; TREHALOSE; UNCLASSIFIED DRUG; WHIB1 PROTEIN; WHIB4 PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL CYCLE; CONTROLLED STUDY; DNA HYBRIDIZATION; DNA MICROARRAY; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SYNTHESIS; GENE CONTROL; GENETIC STRAIN; GENETIC SUSCEPTIBILITY; GENETIC TRANSCRIPTION; GENOME; MICROARRAY ANALYSIS; MOLECULAR GENETICS; MYCOBACTERIUM SMEGMATIS; NONHUMAN; OSMOREGULATION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROCESSING; RNA EXTRACTION; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOT TEMPERATURE; MYCOBACTERIUM SMEGMATIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; REGULON; SIGMA FACTOR;

CORYNEBACTERINEAE; MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS;

EID: 77952046005     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00035-10     Document Type: Article

References (42)

1. Almiron, M., A. J. Link, D. Furlong, and R. Kolter. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:2646-2654. (Pubitemid 23052891)
2. Antelmann, H., S. Engelmann, R. Schmid, A. Sorokin, A. Lapidus, and M. Hecker. 1997. Expression of a stress- and starvation-induced dps/pexBhomologous gene is controlled by the alternative sigma factor sigmaB in Bacillus subtilis. J. Bacteriol. 179:7251-7256. (Pubitemid 27509960)
3. Arguelles, J. C. 2000. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch. Microbiol. 174:217-224.
4. Beaucher, J., S. Rodrigue, P. E. Jacques, I. Smith, R. Brzezinski, and L. Gaudreau. 2002. Novel Mycobacterium tuberculosis anti-sigma factor antagonists control SigmaF activity by distinct mechanisms. Mol. Microbiol. 45:1527-1540.
5. 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.
6. Chowdhury, R. P., S. Gupta, and D. Chatterji. 2007. Identification and characterization of the dps promoter of Mycobacterium smegmatis: promoter recognition by stress-specific extracytoplasmic function sigma factors SigmaH and SigmaF. J. Bacteriol. 189:8973-8981.
7. Crooks, G. E., G. Hon, J. M. Chandonia, and S. E. Brenner. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
8. 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. (Pubitemid 28019782)
9. DeMaio, J., Y. Zhang, C. Ko, D. B. Young, and W. R. Bishai. 1996. A stationary-phase stress-response sigma factor from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 93:2790-2794.
10. De Smet, K. A., A. Weston, I. N. Brown, D. B. Young, and B. D. Robertson. 2000. Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146:199-208.
11. Elbein, A. D., Y. T. Pan, I. Pastuszak, and D. Carroll. 2003. New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R-27R.
12. Gebhard, S., A. Hümpel, A. D. McLellan, and G. M. Cook. 2008. The alternative sigma factor SigF of Mycobacterium smegmatis is required for survival of heat shock, acidic pH and oxidative stress. Microbiology 154:2786-2795.
13. 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.
14. Geiman, D. E., T. R. Raghunand, N. Agarwal, and W. R. Bishai. 2006. Differential gene expression in response to exposure to antimycobacterial agents and other stress conditions among seven Mycobacterium tuberculosis whiB-like genes. Antimicrob. Agents Chemother. 50:2836-2841.
15. Gruber, T. M., and C. A. Gross. 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57:441-466.
16. Gupta, S., and D. Chatterji. 2005. Stress responses in mycobacteria. IUBMB Life 57:149-159.
17. Gupta, S., S. B. Pandit, N. Srinivasan, and D. Chatterji. 2002. Proteomics analysis of carbon-starved Mycobacterium smegmatis: induction of Dps-like protein. Protein Eng. 15:503-512.
18. Holtmann, G., and E. Bremer. 2004. Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters. J. Bacteriol. 186:1683-1693.
19. Kappes, R. M., B. Kempf, and E. Bremer. 1996. Three transport systems for the osmoprotectant glycine betaine operate in Bacillus subtilis: characterization of OpuD. J. Bacteriol. 178:5071-5079.
20. 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.
21. Kim, T. H., J. S. Park, H. J. Kim, Y. Kim, P. Kim, and H. S. Lee. 2005. The whcE gene of Corynebacterium glutamicum is important for survival following heat and oxidative stress. Biochem. Biophys. Res. Commun. 337:757-764.
22. Letunic, I., T. Doerks, and P. Bork. 2009. SMART 6: recent updates and new developments. Nucleic Acids Res. 37:D229-D232.
23. Manganelli, R., R. Provvedi, S. Rodrigue, J. Beaucher, L. Gaudreau, and I. Smith. 2004. Sigma factors and global gene regulation in Mycobacterium tuberculosis. J. Bacteriol. 186:895-902.
24. Münch, R. H., K. A. Grote, M. Scheer, J. Klein, M. Schobert, and D. Jahn. 2005. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21:4187-4189.
25. Murphy, H. N., G. R. Stewart, V. V. Mischenko, A. S. Apt, R. Harris, M. S. McAlister, P. C. Driscoll, D. B. Young, and B. D. Robertson. 2005. The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis. J. Biol. Chem. 280:14524-14529.
26. Nguyen, L., S. Chinnapapagari, and C. J. Thompson. 2005. FbpA-dependent biosynthesis of trehalose dimycolate is required for the intrinsic multidrug resistance, cell wall structure, and colonial morphology of Mycobacterium smegmatis. J. Bacteriol. 187:6603-6611. (Pubitemid 41356232)
27. Parida, B. K., T. Douglas, C. Nino, and S. Dhandayuthapani. 2005. Interactions of anti-sigma factor antagonists of Mycobacterium tuberculosis in the yeast two-hybrid system. Tuberculosis (Edinb.) 85:347-355.
28. Provvedi, R., D. Kocincova, V. Dona, D. Euphrasie, M. Daffe, G. Etienne, R. Manganelli, and J. M. Reyrat. 2008. SigF controls carotenoid pigment production and affects transformation efficiency and hydrogen peroxide sensitivity in Mycobacterium smegmatis. J. Bacteriol. 190:7859-7863.
29. Rodrigue, S., R. Provvedi, P. E. Jacques, L. Gaudreau, and R. Manganelli. 2006. The sigma factors of Mycobacterium tuberculosis. FEMS Microbiol. Rev. 30:926-941.
30. Sechi, L. A., G. E. Felis, N. Ahmed, D. Paccagnini, D. Usai, S. Ortu, P. Molicotti, and S. Zanetti. 2007. Genome and transcriptome scale portrait of sigma factors in Mycobacterium avium subsp. paratuberculosis. Infect. Genet. Evol. 7:424-432.
31. Singh, A. K., and B. N. Singh. 2008. Conservation of Sigma F in mycobacteria and its expression in Mycobacterium smegmatis. Curr. Microbiol. 56:574-580.
32. Singh, A. K., and B. N. Singh. 2009. Differential expression of sigH paralogs during growth and under different stress conditions in Mycobacterium smegmatis. J. Bacteriol. 191:2888-2893.
33. Snapper, S. B., R. E. Melton, S. Mustafa, T. Kieser, and W. R. Jacobs, Jr. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
34. Soliveri, J. A., J. Gomez, W. R. Bishai, and K. F. Chater. 2000. Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other actinomycetes. Microbiology 146:333-343.
35. Staron, A., H. J. Sofia, S. Dietrich, L. E. Ulrich, H. Liesegang, and T. Mascher. 2009. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol. Microbiol. 74:557-581.
36. Villas-Boas, S. G., and P. Bruheim. 2007. Cold glycerol-saline: the promising quenching solution for accurate intracellular metabolite analysis of microbial cells. Anal. Biochem. 370:87-97.
37. von Blohn, C., B. Kempf, R. M. Kappes, and E. Bremer. 1997. Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B. Mol. Microbiol. 25:175-187.
38. Waagmeester, A., J. Thompson, and J. M. Reyrat. 2005. Identifying sigma factors in Mycobacterium smegmatis by comparative genomic analysis. Trends Microbiol. 13:505-509.
39. Walters, S. B., E. Dubnau, I. Kolesnikova, F. Laval, M. Daffe, and I. Smith. 2006. The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol. Microbiol. 60:312-330.
40. 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.
41. Woodruff, P. J., B. L. Carlson, B. Siridechadilok, M. R. Pratt, R. H. Senaratne, J. D. Mougous, L. W. Riley, S. J. Williams, and C. R. Bertozzi. 2004. Trehalose is required for growth of Mycobacterium smegmatis. J. Biol. Chem. 279:28835-28843.
42. Ziegelhoffer, E. C., and T. J. Donohue. 2009. Bacterial responses to photooxidative stress. Nat. Rev. Microbiol. 7:856-863.