Assessment of transcriptional responses of Bacillus subtilis cells to the antibiotic enduracidin, which interferes with cell wall synthesis, using a high-density tiling chip

Genes and Genetic Systems

Volumn 84, Issue 4, 2009, Pages 253-267

  Rukmana, Andriansjah ^a   Morimoto, Takuya ^a,b   Takahashi, Hiroki ^a   Giyanto, ^a,c   Ogasawara, Naotake ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b KAO CORPORATION   (Japan)

^c BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

Author keywords

Bacillus subtilis; Bacitracin; Enduracidin; LiaHI; LiaRS; SigM; Spx

Indexed keywords

ANTIBIOTIC AGENT; BACITRACIN; ENRAMYCIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CYCLOPEPTIDE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BACTERIAL GENETICS; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC TRANSCRIPTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN INDUCTION; REGULON; UPREGULATION; BIOSYNTHESIS; CELL WALL; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

BACILLUS SUBTILIS; POSIBACTERIA;

ANTI-INFECTIVE AGENTS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL WALL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDES, CYCLIC; SIGNAL TRANSDUCTION;

EID: 75749157428     PISSN: 13417568     EISSN: None     Source Type: Journal    
DOI: 10.1266/ggs.84.253     Document Type: Article

References (44)

1. Asai, K., Ishiwata, K., Matsuzaki, K., and Sadaie, Y. (2008) A viable Bacillus subtilis strain without functional extracytoplasmic function sigma genes. J. Bacteriol. 190, 2633-2636.
2. Bernard, R., El Ghachi, M., Mengin-Lecreulx, D., Chippaux, M., and Denizot, F. (2005) BcrC from Bacillus subtilis acts as an undecaprenyl pyrophosphate phosphatase in bacitracin resistance. J. Biol. Chem. 280, 28852-28857.
3. Bernard, R., Guiseppi, A., Chippaux, M., Foglino, M., and Denizot, F. (2007) Resistance to bacitracin in Bacillus subtilis: unexpected requirement of the BceAB ABC transporter in the control of expression of its own structural genes. J. Bacteriol. 189, 8636-8642.
4. Butcher, B. G., and 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.
5. Cao, M., and Helmann, J. D. (2002) Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors. J. Bacteriol. 184, 6123-6129.
6. Cao, M., and Helmann, J. D. (2004) The Bacillus subtilis extracytoplasmic-function sigmaX factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J. Bacteriol. 186, 1136-1146.
7. Cao, M., Wang, T., Ye, R., and Helmann, J. D. (2002) Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis sigmaW and sigmaM regulons. Mol. Microbiol. 45, 1267-1276.
8. Cao, M., Moore, C. M., and Helmann, J. D. (2005) Bacillus subtilis paraquat resistance is directed by sigmaM, an extracytoplasmic function sigma factor, and is conferred by YqjL and BcrC. J. Bacteriol. 187, 2948-2956.
9. Darmon, E., Noone, D., Masson, A., Bron, S., Kuipers, O. P., Devine, K. M., and van Dijl, J. M. (2002) A novel class of heat and secretion stress-responsive genes is controlled by the autoregulated CssRS two-component system of Bacillus subtilis. J. Bacteriol. 184, 5661-5671.
10. Duy, N. V., Mader, U., Tran, N. P., Cavin, J. F., Tam le, T., Albrecht, D., Hecker, M., and Antelmann, H. (2007) The proteome and transcriptome analysis of Bacillus subtilis in response to salicylic acid. Proteomics 7, 698-710.
11. Eiamphungporn, W., and Helmann, J. D. (2008) The Bacillus subtilis sigmaM regulon and its contribution to cell envelope stress responses. Mol. Microbiol. 67, 830-848.
12. Fang, X., Tiyanont, K., Zhang, Y., Wanner, J., Boger, D., and Walker, S. (2006) The mechanism of action of ramoplanin and enduracidin. Mol. Biosyst. 2, 69-76.
13. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
14. Hachmann, A. B., Angert, E. R., and Helmann, J. D. (2009) Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob. Agents Chemother. 53, 1598-1609.
15. Hansen, M. E., Mijakovic, I., Jensen, P. R., and Sibbesen, O. (2007) Use of Bacillus subtilis for the biosynthesis of nisin. 4th International Conference on Functional Genomics of Gram-positive Microorganisms, Pisa, Italy.
16. Higashide, E., Hatano, K., Shibata, M., and Nakazawa, K. (1968) Enduracidin, a new antibiotic. I. Streptomyces fungicidicus No. B5477, an enduracidin producing organism. J. Antibiot. (Tokyo) 21, 126-137.
17. Hoper, D., Volker, U., and Hecker, M. (2005) Comprehensive characterization of the contribution of individual SigB-dependent general stress genes to stress resistance of Bacillus subtilis. J. Bacteriol. 187, 2810-2826.
18. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B., and Speed, T. P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15.
19. Ishikawa, S., Kawai, Y., Hiramatsu, K., Kuwano, M., and Ogasawara, N. (2006) A new FtsZ-interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis. Mol. Microbiol. 60, 1364-1380.
20. Ishikawa, S., Ogura, Y., Yoshimura, M., Okumura, H., Cho, E., Kawai, Y., Kurokawa, K., Oshima, T., and Ogasawara, N. (2007) Distribution of stable DnaA-binding sites on the Bacillus subtilis genome detected using a modified ChIP-chip method. DNA Res. 14, 155-168.
21. Jordan, S., Junker, A., Helmann, J.D., and 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 stresssensing two-component system. J. Bacteriol. 188, 5153-5166.
22. Jordan, S., Hutchings, M. I., and Mascher, T. (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol. Rev. 32, 107-146.
23. Joseph, P., Guiseppi, A., Sorokin, A., and Denizot, F. (2004) Characterization of the Bacillus subtilis YxdJ response regulator as the inducer of expression for the cognate ABC transporter YxdLM. Microbiology 150, 2609-2617.
24. Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G., Andersen, K. K., Arnaud, M., Asai, K., Ashikaga, S., Aymerich, S., Bessieres, P., et al. (2003) Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100, 4678-4683.
25. Kobayashi, R., Suzuki, T., and Yoshida, M. (2007) Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66, 100-109.
26. Mascher, T. (2006) Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol. Lett. 264, 133-144.
27. Mascher, T., Margulis, N. G., Wang, T., Ye, R. W., and Helmann, J. D. (2003) Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol. Microbiol. 50, 1591-1604.
28. Mascher, T., Zimmer, S.L., Smith, T. A., and 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.
29. Mascher, T., Hachmann, A. B., and Helmann, J. D. (2007) Regulatory overlap and functional redundancy among Bacillus subtilis extracytoplasmic function sigma factors. J. Bacteriol. 189, 6919-6927.
30. Miethke, M., Hecker, M., and Gerth, U. (2006) Involvement of Bacillus subtilis ClpE in CtsR degradation and protein quality control. J. Bacteriol. 188, 4610-4619.
31. Morimoto, T., Kadoya, R., Endo, K, Tohata, M., Sawada, K., Liu, S., Ozawa, T., Kodama, T., Kakeshita, H., Kageyama, Y., et al. (2008) Enhanced recombinant protein productivity by genome reduction in Bacillus subtilis. DNA Res. 15, 73-81.
32. Morimoto, T., Ara, K., Ozaki, K., and Ogasawara, N. (2009) A new simple method to introduce marker-free deletions in the Bacillus subtilis genome. Genes Genet. Syst. 84, 315-318.
33. Muthaiyan, A., Silverman, J. A., Jayaswal, R. K., and Wilkinson, B. J. (2008) Transcriptional profiling reveals that daptomycin induces the Staphylococcus aureus cell wall stress stimulon and genes responsive to membrane depolarization. Antimicrob. Agents Chemother. 52, 980-990.
34. Nakano, S., Kuster-Schock, E., Grossman, A. D., and Zuber, P. (2003) Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 100, 13603-13608.
35. Nguyen, V. D., Wolf, C., Mader, U., Lalk, M., Langer, P., Lindequist, U., Hecker, M., and Antelmann, H. (2007) Transcriptome and proteome analyses in response to 2-methylhy-droquinone and 6-brom-2-vinyl-chroman-4-on reveal different degradation systems involved in the catabolism of aromatic compounds in Bacillus subtilis. Proteomics 7, 1391-1408.
36. Ohki, R., Giyanto, Tateno, K., Masuyama, W., Moriya, S., Kobayashi, K., and Ogasawara, N. (2003) The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol. Microbiol. 49, 1135-1144.
37. Pietiainen, M., Gardemeister, M., Mecklin, M., Leskela, S., Savas, M., and Kontinen, V.P. (2005) Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology 151, 1577-1592.
38. Reyes, D. Y., and Zuber, P. (2008) Activation of transcription initiation by Spx: formation of transcription complex and identification of a Cis-acting element required for transcriptional activation. Mol. Microbiol. 69, 765-779.
39. Rietkotter, E., Hoyer, D., and Mascher, T. (2008) Bacitracin sensing in Bacillus subtilis. Mol. Microbiol. 68, 768-785.
40. Tseng, C. L., and Shaw, G. C. (2008) Genetic evidence for the actin homolog gene mreBH and the bacitracin resistance gene bcrC as targets of the alternative sigma factor Sigl of Bacillus subtilis. J. Bacteriol. 190, 1561-1567.
41. Wang, Z., Gerstein, M., and Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63.
42. Wecke, T., Zuhlke, D., Mader, U., Jordan, S., Voigt, B., Pelzer, S., Labischinski, H., Homuth, G., Hecker, M., and Mascher, T. (2009) Daptomycin versus Friulimicin B: in-depth profiling of Bacillus subtilis cell envelope stress responses. Anti-microb. Agents Chemother. 53, 1619-1623.
43. Yin, X., and Zabriskie, T.M. (2006) The enduracidin biosynthetic gene cluster from Streptomyces fungicidicus. Microbiology 152, 2969-2983.
44. Zhang, X. Z., Yan, X., Cui, Z. L., Hong, Q., and Li, S. P. (2006) mazF, a novel counter-selectable marker for unmarked chromosomal manipulation in Bacillus subtilis. Nucleic Acids Res. 34, e71.