1887

Abstract

Maintaining envelope integrity is crucial for the survival of any bacterial cell, especially those living in a complex and ever-changing habitat such as the soil ecosystem. The LiaRS two-component system is part of the regulatory network orchestrating the cell-envelope stress response in . It responds to perturbations of the cell envelope, especially the presence of antibiotics that interfere with the lipid II cycle, such as bacitracin or vancomycin. LiaRS-dependent regulation is strictly repressed by the membrane protein LiaF in the absence of inducing conditions. Here, it is shown that the LiaR-dependent promoter is induced at the onset of stationary phase without addition of exogenous stresses. Its activity is embedded in the complex regulatory cascade governing adaptation at the onset of stationary phase. The promoter is directly repressed by the transition state regulator AbrB and responds indirectly to the activity of Spo0A, the master regulator of sporulation. The activity of the promoter is therefore tightly regulated by at least five regulators to ensure an appropriate level of expression.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/006817-0
2007-08-01
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/8/2530.html?itemId=/content/journal/micro/10.1099/mic.0.2007/006817-0&mimeType=html&fmt=ahah

References

  1. Adams H., Teertstra W., Demmers J., Boesten R., Tommassen J. 2003; Interactions between phage-shock proteins in Escherichia coli . J Bacteriol 185:1174–1180
    [Google Scholar]
  2. Arnaud M., Chastanet A., Debarbouille M. 2004; New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl Environ Microbiol 70:6887–6891
    [Google Scholar]
  3. Bobay B. G., Benson L., Naylor S., Feeney B., Clark A. C., Goshe M. B., Strauch M. A., Thompson R., Cavanagh J. 2004; Evaluation of the DNA binding tendencies of the transition state regulator AbrB. Biochemistry 43:16106–16118
    [Google Scholar]
  4. Bobay B. G., Mueller G. A., Thompson R. J., Murzin A. G., Venters R. A., Strauch M. A., Cavanagh J. 2006; NMR structure of AbhN and comparison with AbrBN: first insights into the DNA binding promiscuity and specificity of AbrB-like transition state regulator proteins. J Biol Chem 281:21399–21409
    [Google Scholar]
  5. Bordes P., Wigneshweraraj S. R., Schumacher J., Zhang X., Chaney M., Buck M. 2003; The ATP hydrolyzing transcription activator phage shock protein F of Escherichia coli : identifying a surface that binds σ 54 . Proc Natl Acad Sci U S A 100:2278–2283
    [Google Scholar]
  6. Brissette J. L., Russel M., Weiner L., Model P. 1990; Phage shock protein, a stress protein of Escherichia coli . Proc Natl Acad Sci U S A 87:862–866
    [Google Scholar]
  7. Darwin A. J. 2005; The phage-shock-protein response. Mol Microbiol 57:621–628
    [Google Scholar]
  8. Dworkin J., Jovanovic G., Model P. 2000; The PspA protein of Escherichia coli is a negative regulator of σ 54-dependent transcription. J Bacteriol 182:311–319
    [Google Scholar]
  9. Errington J. 2003; Regulation of endospore formation in Bacillus subtilis . Nat Rev Microbiol 1:117–126
    [Google Scholar]
  10. Fawcett P., Eichenberger P., Losick R., Youngman P. 2000; The transcriptional profile of early to middle sporulation in Bacillus subtilis . Proc Natl Acad Sci U S A 97:8063–8068
    [Google Scholar]
  11. Fujita M., Gonzalez-Pastor J. E., Losick R. 2005; High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis . J Bacteriol 187:1357–1368
    [Google Scholar]
  12. Guerout-Fleury A. M., Shazand K., Frandsen N., Stragier P. 1995; Antibiotic-resistance cassettes for Bacillus subtilis . Gene 167:335–336
    [Google Scholar]
  13. Haas W., Kaushal D., Sublett J., Obert C., Tuomanen E. I. 2005; Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae . J Bacteriol 187:8205–8210
    [Google Scholar]
  14. Hamon M. A., Stanley N. R., Britton R. A., Grossman A. D., Lazazzera B. A. 2004; Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis . Mol Microbiol 52:847–860
    [Google Scholar]
  15. Harwood C. R., Cutting S. M. 1990 Molecular Biological Methods for Bacillus Chichester: Wiley;
  16. Hyyryläinen H. L., Sarvas M., Kontinen V. P. 2005; Transcriptome analysis of the secretion stress response of Bacillus subtilis . Appl Microbiol Biotechnol 67:389–396
    [Google Scholar]
  17. 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
    [Google Scholar]
  18. Kleerebezem M., Tommassen J. 1993; Expression of the pspA gene stimulates efficient protein export in Escherichia coli . Mol Microbiol 7:947–956
    [Google Scholar]
  19. Kleerebezem M., Crielaard W., Tommassen J. 1996; Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J 15:162–171
    [Google Scholar]
  20. Kobayashi H., Yamamoto M., Aono R. 1998; Appearance of a stress-response protein, phage-shock protein A, in Escherichia coli exposed to hydrophobic organic solvents. Microbiology 144:353–359
    [Google Scholar]
  21. Kovács M., Halfmann A., Fedtke I., Heintz M., Peschel A., Vollmer W., Hakenbeck R., Brückner R. 2006; A functional dlt operon, encoding proteins required for incorporation of d-alanine in teichoic acids in Gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae . J Bacteriol 188:5797–5805
    [Google Scholar]
  22. Kuroda M., Kuroda H., Oshima T., Takeuchi F., Mori H., Hiramatsu K. 2003; Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus . Mol Microbiol 49:807–821
    [Google Scholar]
  23. Mascher T. 2006; Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol Lett 264:133–144
    [Google Scholar]
  24. 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
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  27. Msadek T. 1999; When the going gets tough: survival strategies and environmental signaling networks in Bacillus subtilis . Trends Microbiol 7:201–207
    [Google Scholar]
  28. Ogura M., Shimane K., Asai K., Ogasawara N., Tanaka T. 2003; Binding of response regulator DegU to the aprE promoter is inhibited by RapG, which is counteracted by extracellular PhrG in Bacillus subtilis . Mol Microbiol 49:1685–1697
    [Google Scholar]
  29. Ogura M., Matsuzawa A., Yoshikawa H., Tanaka T. 2004; Bacillus subtilis SalA (YbaL) negatively regulates expression of scoC , which encodes the repressor for the alkaline exoprotease gene, aprE . J Bacteriol 186:3056–3064
    [Google Scholar]
  30. Peschel A., Otto M., Jack R. W., Kalbacher H., Jung G., Götz F. 1999; Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274:8405–8410
    [Google Scholar]
  31. Peters J. E., Craig N. L. 2001; Tn7: smarter than we thought. Nat Rev Mol Cell Biol 2:806–814
    [Google Scholar]
  32. Petersohn A., Brigulla M., Haas S., Hoheisel J. D., Volker U., Hecker M. 2001; Global analysis of the general stress response of Bacillus subtilis . J Bacteriol 183:5617–5631
    [Google Scholar]
  33. Phillips Z. E., Strauch M. A. 2002; Bacillus subtilis sporulation and stationary phase gene expression. Cell Mol Life Sci 59:392–402
    [Google Scholar]
  34. Pietiäinen 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 sigma factors and two-component signal transduction systems. Microbiology 151:1577–1592
    [Google Scholar]
  35. Sambrook J., Russell D. W. 2001 Molecular Cloning – a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  36. Sapolsky R., Iyer P., Caldwell B., Weyler W., Chotani G., Ferrari E. 2005; Bacillus subtilis "Chronotranscriptomics": twenty-six time-points of transcript profiling from mid-exponential to post-transition phase. In Abstracts of 3rd Conference on Functional Genomics of Gram-Positive Micro-organisms June 12–16 2005 San Diego, California: abstract T18
    [Google Scholar]
  37. Schaeffer P., Millet J., Aubert J. P. 1965; Catabolic repression of bacterial sporulation. Proc Natl Acad Sci U S A 54:704–711
    [Google Scholar]
  38. Shafikhani S. H., Partovi A. A., Leighton T. 2003; Catabolite-induced repression of sporulation in Bacillus subtilis . Curr Microbiol 47:300–308
    [Google Scholar]
  39. Silver L. L. 2003; Novel inhibitors of bacterial cell wall synthesis. Curr Opin Microbiol 6:431–438
    [Google Scholar]
  40. Silver L. L. 2006; Does the cell wall of bacteria remain a viable source of targets for novel antibiotics?. Biochem Pharmacol 71:996–1005
    [Google Scholar]
  41. Stanley N. R., Britton R. A., Grossman A. D., Lazazzera B. A. 2003; Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951–1957
    [Google Scholar]
  42. Stein T. 2005; Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857
    [Google Scholar]
  43. Steinmetz M., Richter R. 1994; Easy cloning of mini-Tn10 insertions from the Bacillus subtilis chromosome. J Bacteriol 176:1761–1763
    [Google Scholar]
  44. Strauch M. A., Spiegelman G. B., Perego M., Johnson W. C., Burbulys D., Hoch J. A. 1989; The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein. EMBO J 8:1615–1621
    [Google Scholar]
  45. Strauch M., Webb V., Spiegelman G., Hoch J. A. 1990; The Spo0A protein of Bacillus subtilis is a repressor of the abrB gene. Proc Natl Acad Sci U S A 87:1801–1805
    [Google Scholar]
  46. Szurmant H., Mohan M. A., Imus P. M., Hoch J. A. 2007; YycH and YycI interact to regulate the essential YycFG two-component system in Bacillus subtilis . J Bacteriol 189:3280–3289
    [Google Scholar]
  47. Tam le T., Eymann C., Albrecht D., Sietmann R., Schauer F., Hecker M., Antelmann H. 2006; Differential gene expression in response to phenol and catechol reveals different metabolic activities for the degradation of aromatic compounds in Bacillus subtilis . Environ Microbiol 8:1408–1427
    [Google Scholar]
  48. Vagner V., Dervyn E., Ehrlich S. D. 1998; A vector for systematic gene inactivation in Bacillus subtilis . Microbiology 144:3097–3104
    [Google Scholar]
  49. Wach A. 1996; PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in Scerevisiae. Yeast 12:259–265
    [Google Scholar]
  50. Walsh C. 2003 Antibiotics – Actions, Origins Resistance Washington, DC: American Society for Microbiology;
    [Google Scholar]
  51. 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
    [Google Scholar]
  52. Weiner L., Model P. 1994; Role of an Escherichia coli stress-response operon in stationary-phase survival. Proc Natl Acad Sci U S A 91:2191–2195
    [Google Scholar]
  53. Wiegert T., Homuth G., Versteeg S., Schumann W. 2001; Alkaline shock induces the Bacillus subtilis σ W regulon. Mol Microbiol 41:59–71
    [Google Scholar]
  54. Xu K., Strauch M. A. 1996; In vitro selection of optimal AbrB-binding sites: comparison to known in vivo sites indicates flexibility in AbrB binding and recognition of three-dimensional DNA structures. Mol Microbiol 19:145–158
    [Google Scholar]
  55. Youngman P. 1990; Use of transposons and integrational vectors for mutagenesis and construction of gene fusions in Bacillus subtilis . In Molecular Biological Methods for Bacillus pp 221–266 Edited by Harwood S. M., Cutting C. R. Chichester: Wiley;
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.2007/006817-0
Loading
/content/journal/micro/10.1099/mic.0.2007/006817-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error