1887

Abstract

Lipoteichoic acid (LTA) is an important cell envelope component of Gram-positive bacteria. has four homologous genes for LTA synthesis: (), , and . The products LtaS (YflE), YfnI and YqgS are bona fide LTA synthetases, whereas YvgJ functions only as an LTA primase. To clarify whether defects in LTA on the cell envelope trigger extracytoplasmic function (ECF) sigma factors, mRNA levels of the autoregulated ECF sigma factors in cells with singly and multiply deleted alleles of the homologues were examined by real-time RT-PCR. This revealed that and were induced in cells with a null allele of Δ and Δ, respectively, and that no ECF sigma factor was induced in cells with a single null allele of Δ or Δ. In cells with double null alleles (Δ and Δ), and were induced in addition to and . Cells with triple null alleles (Δ Δ and Δ) showed a pattern of induction similar to that of the double null. In cells with quadruple null alleles, and were newly induced. Cells with Δ had approximatley 1/4 the diglucosyldiacylglycerol and over 10 times the CDP-diacylglycerol of wild-type cells. Compensatory elevation of the mRNA level of other homologues was observed (in Δ cells the level of was elevated; in Δ cells that of and was elevated; both were even higher in Δ Δ cells). In Δ cells, the mRNA level of was corroborated to be regulated by σ, which is activated in the null mutant cells. In Δ cells, the mRNA levels of and reverted to less than those of wild-type when a defective allele was introduced. Since was activated in cells with Δ, this suggests that the induction of and is dependent on σ. The LTAs produced by the four homologues seem to play distinct physiological roles to maintain the full function of LTA on the cell envelope.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.063420-0
2013-01-01
2021-07-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/1/23.html?itemId=/content/journal/micro/10.1099/mic.0.063420-0&mimeType=html&fmt=ahah

References

  1. Anagnostopoulos C., Crawford I. P. ( 1961). Transformation studies on the linkage of markers in the tryptophan pathway in Bacillus subtilis . Proc Natl Acad Sci U S A 47:378–390 [View Article][PubMed]
    [Google Scholar]
  2. Asai K., Matsumoto T., Sadaie Y. ( 2005). ECF (extracytoplasmic function) sigma factors of Bacillus subtilis . Survival and Death in Bacteria143–153 Yamada M. Kerala, India: Research Signpost;
    [Google Scholar]
  3. Asai K., Ishiwata K., Matsuzaki K., Sadaie Y. ( 2008). A viable Bacillus subtilis strain without functional extracytoplasmic function sigma genes. J Bacteriol 190:2633–2636 [View Article][PubMed]
    [Google Scholar]
  4. Bligh E. G., Dyer W. J. ( 1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917 [View Article][PubMed]
    [Google Scholar]
  5. Butcher B. G., Helmann J. D. ( 2006). Identification of Bacillus subtilis σ-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli . Mol Microbiol 60:765–782 [View Article][PubMed]
    [Google Scholar]
  6. Cao M., 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 [View Article][PubMed]
    [Google Scholar]
  7. Cao M., Wang T., Ye R., Helmann J. D. ( 2002). Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis σW and σM regulons. Mol Microbiol 45:1267–1276 [View Article][PubMed]
    [Google Scholar]
  8. Cao M., Salzberg L., Tsai C. S., Mascher T., Bonilla C., Wang T., Ye R. W., Márquez-Magaña L., Helmann J. D. ( 2003). Regulation of the Bacillus subtilis extracytoplasmic function protein σY and its target promoters. J Bacteriol 185:4883–4890 [View Article][PubMed]
    [Google Scholar]
  9. Cronan J. E. ( 2003). Bacterial membrane lipids: where do we stand?. Annu Rev Microbiol 57:203–224 [View Article][PubMed]
    [Google Scholar]
  10. De Mendoza D., Schujman G. E., Aguilar P. S. ( 2002). Biosynthesis and function of membrane lipids. Bacillus subtilis and its Closest Relatives43–55 Sonenshein A. L., Hoch J. A., Losick R. Washington, D C.: American Society for Microbiology; [CrossRef]
    [Google Scholar]
  11. Eiamphungporn W., Helmann J. D. ( 2008). The Bacillus subtilis σM regulon and its contribution to cell envelope stress responses. Mol Microbiol 67:830–848 [View Article][PubMed]
    [Google Scholar]
  12. Gründling A., Schneewind O. ( 2007a). Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus . J Bacteriol 189:2521–2530 [View Article][PubMed]
    [Google Scholar]
  13. Gründling A., Schneewind O. ( 2007b). Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus . Proc Natl Acad Sci U S A 104:8478–8483 [View Article][PubMed]
    [Google Scholar]
  14. Guariglia-Oropeza V., Helmann J. D. ( 2011). Bacillus subtilis σV confers lysozyme resistance by activation of two cell wall modification pathways, peptidoglycan O-acetylation and D-alanylation of teichoic acids. J Bacteriol 193:6223–6232 [View Article][PubMed]
    [Google Scholar]
  15. Hashimoto M., Takahashi H., Hara Y., Hara H., Asai K., Sadaie Y., Matsumoto K. ( 2009). Induction of extracytoplasmic function sigma factors in Bacillus subtilis cells with membranes of reduced phosphatidylglycerol content. Genes Genet Syst 84:191–198 [View Article][PubMed]
    [Google Scholar]
  16. Helmann J. D. ( 2002). The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110 [View Article][PubMed]
    [Google Scholar]
  17. Ho T. D., Hastie J. L., Intile P. J., Ellermeier C. D. ( 2011). The Bacillus subtilis extracytoplasmic function σ factor σV is induced by lysozyme and provides resistance to lysozyme. J Bacteriol 193:6215–6222 [View Article][PubMed]
    [Google Scholar]
  18. Horsburgh M. J., Moir A. ( 1999). Sigma 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 [View Article][PubMed]
    [Google Scholar]
  19. Jerga A., Lu Y. J., Schujman G. E., de Mendoza D., Rock C. O. ( 2007). Identification of a soluble diacylglycerol kinase required for lipoteichoic acid production in Bacillus subtilis . J Biol Chem 282:21738–21745 [View Article][PubMed]
    [Google Scholar]
  20. 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 [View Article][PubMed]
    [Google Scholar]
  21. Kawai F., Shoda M., Harashima R., Sadaie Y., Hara H., Matsumoto K. ( 2004). Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186:1475–1483 [View Article][PubMed]
    [Google Scholar]
  22. Kiriukhin M. Y., Debabov D. V., Shinabarger D. L., Neuhaus F. C. ( 2001). Biosynthesis of the glycolipid anchor in lipoteichoic acid of Staphylococcus aureus RN4220: role of YpfP, the diglucosyldiacylglycerol synthase. J Bacteriol 183:3506–3514 [View Article][PubMed]
    [Google Scholar]
  23. Kobayashi K., Ehrlich S. D., Albertini A., Amati G., Andersen K. K., Arnaud M., Asai K., Ashikaga S., Aymerich S. & other authors ( 2003). Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100:4678–4683 [View Article][PubMed]
    [Google Scholar]
  24. Koch H. U., Haas R., Fischer W. ( 1984). The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus . Eur J Biochem 138:357–363 [View Article][PubMed]
    [Google Scholar]
  25. Kosono S., Asai K., Sadaie Y., Kudo T. ( 2004). Altered gene expression in the transition phase by disruption of a Na+/H+ antiporter gene (shaA) in Bacillus subtilis . FEMS Microbiol 232:93–99 [View Article]
    [Google Scholar]
  26. Luo Y., Helmann J. D. ( 2012). Analysis of the role of Bacillus subtilis σM in β-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol Microbiol 83:623–639 [View Article][PubMed]
    [Google Scholar]
  27. Matsumoto K., Okada M., Horikoshi Y., Matsuzaki H., Kishi T., Itaya M., Shibuya I. ( 1998). Cloning, sequencing, and disruption of the Bacillus subtilis psd gene coding for phosphatidylserine decarboxylase. J Bacteriol 180:100–106[PubMed]
    [Google Scholar]
  28. Matsumoto K., Kusaka J., Nishibori A., Hara H. ( 2006). Lipid domains in bacterial membranes. Mol Microbiol 61:1110–1117 [View Article][PubMed]
    [Google Scholar]
  29. Matsumoto K., Matsuoka S., Hara H. ( 2012). Membranes and lipids. Escherichia coli and Bacillus subtilis: The Frontiers of Molecular Microbiology Revisited61–91 Sadaie Y., Matsumoto K. Kerala, India: Research Signpost;
    [Google Scholar]
  30. Matsumoto T., Nakanishi K., Asai K., Sadaie Y. ( 2005). Transcriptional analysis of the ylaABCD operon of Bacillus subtilis encoding a sigma factor of extracytoplasmic function family. Genes Genet Syst 80:385–393 [View Article][PubMed]
    [Google Scholar]
  31. Matsuoka S., Chiba M., Tanimura Y., Hashimoto M., Hara H., Matsumoto K. ( 2011a). Abnormal morphology of Bacillus subtilis ugtP mutant cells lacking glucolipids. Genes Genet Syst 86:295–304 [View Article][PubMed]
    [Google Scholar]
  32. Matsuoka S., Hashimoto M., Kamiya Y., Miyazawa T., Ishikawa K., Hara H., Matsumoto K. ( 2011b). The Bacillus subtilis essential gene dgkB is dispensable in mutants with defective lipoteichoic acid synthesis. Genes Genet Syst 86:365–376 [View Article][PubMed]
    [Google Scholar]
  33. Morimoto T., Ara K., Ozaki K., Ogasawara N. ( 2009). A new simple method to introduce marker-free deletions in the Bacillus subtilis genome. Genes Genet Syst 84:315–318 [View Article][PubMed]
    [Google Scholar]
  34. Murray E. J., Stanley-Wall N. R. ( 2010). The sensitivity of Bacillus subtilis to diverse antimicrobial compounds is influenced by Abh. Arch Microbiol 192:1059–1067 [View Article][PubMed]
    [Google Scholar]
  35. Neuhaus F. C., Baddiley J. ( 2003). A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67:686–723 [View Article][PubMed]
    [Google Scholar]
  36. Nishibori A., Kusaka J., Hara H., Umeda M., Matsumoto K. ( 2005). Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 187:2163–2174 [View Article][PubMed]
    [Google Scholar]
  37. Petersohn A., Brigulla M., Haas S., Hoheisel J. D., Völker U., Hecker M. ( 2001). Global analysis of the general stress response of Bacillus subtilis . J Bacteriol 183:5617–5631 [View Article][PubMed]
    [Google Scholar]
  38. Ryu H.-B., Shin I., Yim H.-S., Kang S. O. ( 2006). YlaC is an extracytoplasmic function (ECF) sigma factor contributing to hydrogen peroxide resistance in Bacillus subtilis . J Microbiol 44:206–216[PubMed]
    [Google Scholar]
  39. Salzberg L. I., Helmann J. D. ( 2008). Phenotypic and transcriptomic characterization of Bacillus subtilis mutants with grossly altered membrane composition. J Bacteriol 190:7797–7807 [View Article][PubMed]
    [Google Scholar]
  40. Schirner K., Marles-Wright J., Lewis R. J., Errington J. ( 2009). Distinct and essential morphogenic functions for wall- and lipo-teichoic acids in Bacillus subtilis . EMBO J 28:830–842 [View Article][PubMed]
    [Google Scholar]
  41. Sutcliffe I. C. ( 2011). Priming and elongation: dissection of the lipoteichoic acid biosynthetic pathway in Gram-positive bacteria. Mol Microbiol 79:553–556 [View Article][PubMed]
    [Google Scholar]
  42. Thackray P. D., Moir A. ( 2003). SigM, 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 [View Article][PubMed]
    [Google Scholar]
  43. Tojo S., Matsunaga M., Matsumoto T., Kang C. M., Yamaguchi H., Asai K., Sadaie Y., Yoshida K., Fujita Y. ( 2003). Organization and expression of the Bacillus subtilis sigY operon. J Biochem 134:935–946 [View Article][PubMed]
    [Google Scholar]
  44. Wang P.-Z., Doi R. H. ( 1984). Overlapping promoters transcribed by Bacillus subtilis σ55 and σ37 RNA polymerase holoenzymes during growth and stationary phases. J Biol Chem 259:8619–8625[PubMed]
    [Google Scholar]
  45. Wörmann M. E., Corrigan R. M., Simpson P. J., Matthews S. J., Gründling A. ( 2011). Enzymatic activities and functional interdependencies of Bacillus subtilis lipoteichoic acid synthesis enzymes. Mol Microbiol 79:566–583 [View Article][PubMed]
    [Google Scholar]
  46. Yoshimura M., Asai K., Sadaie Y., Yoshikawa H. ( 2004). Interaction of Bacillus subtilis extracytoplasmic function (ECF) sigma factors with the N-terminal regions of their potential anti-sigma factors. Microbiology 150:591–599 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.063420-0
Loading
/content/journal/micro/10.1099/mic.0.063420-0
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