1887

Abstract

-Alanyl esters on lipoteichoic acid (LTA) are involved in adhesion, biofilm formation, resistance to cationic antimicrobial peptides, and immune stimulation. There is evidence that bacteria can modulate the level of -alanyl esters on LTA in response to challenge, but the mechanism of regulation appears to be different among bacteria. In this study, expression of the operon responsible for -alanylation of LTA was examined in the commensal bacterium . expression was assessed using the promoter– reporter gene assay, LTA -alanine content measurements and mRNA quantification. The results showed that expression was growth phase-dependent, with the greatest expression at the mid-exponential phase of growth. In contrast to , expression in was not affected by the exogenous addition of Mg or K. Interestingly, expression was upregulated under acidic conditions or when cells were stressed with polymyxin B, indicating that cell envelope stress may be a signal for expression. In view of these results, mutants defective in the cell envelope stress LiaSR two-component regulatory system were constructed. The and mutants showed an increase in expression over the parent strain at neutral pH. The mutants failed to respond to low pH and polymyxin B stress; expression remained the same in the presence or absence of these stresses. These results suggest that expression in is regulated by the LiaSR regulatory system in response to environmental signals such as pH and polymyxin B. The regulation appears to be complex, involving both repression and activation mechanisms.

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2011-08-01
2019-11-22
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References

  1. Abachin E. , Poyart C. , Pellegrini E. , Milohanic E. , Fiedler F. , Berche P. , Trieu-Cuot P. . ( 2002; ). Formation of d-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes . . Mol Microbiol 43:, 1–14. [CrossRef].[PubMed]
    [Google Scholar]
  2. Archibald A. R. , Baddiley J. , Heptinstall S. . ( 1973; ). The alanine ester content and magnesium binding capacity of walls of Staphylococcus aureus H grown at different pH values. . Biochim Biophys Acta 291:, 629–634. [CrossRef].[PubMed]
    [Google Scholar]
  3. Boyd D. A. , Cvitkovitch D. G. , Bleiweis A. S. , Kiriukhin M. Y. , Debabov D. V. , Neuhaus F. C. , Hamilton I. R. . ( 2000; ). Defects in d-alanyl-lipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. . J Bacteriol 182:, 6055–6065. [CrossRef].[PubMed]
    [Google Scholar]
  4. Burne R. A. , Wen Z. T. , Chen Y. Y. , Penders J. E. . ( 1999; ). Regulation of expression of the fructan hydrolase gene of Streptococcus mutans GS-5 by induction and carbon catabolite repression. . J Bacteriol 181:, 2863–2871.[PubMed]
    [Google Scholar]
  5. Chan K. G. , Mayer M. , Davis E. M. , Halperin S. A. , Lin T. J. , Lee S. F. . ( 2007; ). Role of d-alanylation of Streptococcus gordonii lipoteichoic acid in innate and adaptive immunity. . Infect Immun 75:, 3033–3042. [CrossRef].[PubMed]
    [Google Scholar]
  6. Clemans D. L. , Kolenbrander P. E. , Debabov D. V. , Zhang Q. , Lunsford R. D. , Sakone H. , Whittaker C. J. , Heaton M. P. , Neuhaus F. C. . ( 1999; ). Insertional inactivation of genes responsible for the d-alanylation of lipoteichoic acid in Streptococcus gordonii DL1 (Challis) affects intrageneric coaggregations. . Infect Immun 67:, 2464–2474.[PubMed]
    [Google Scholar]
  7. Collins L. V. , Kristian S. A. , Weidenmaier C. , Faigle M. , Van Kessel K. P. , Van Strijp J. A. , Götz F. , Neumeister B. , Peschel A. . ( 2002; ). Staphylococcus aureus strains lacking d-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. . J Infect Dis 186:, 214–219. [CrossRef].[PubMed]
    [Google Scholar]
  8. Ellwood D. C. , Tempest D. W. . ( 1972; ). Effects of environment on bacterial wall content and composition. . Adv Microb Physiol 7:, 83–117. [CrossRef]
    [Google Scholar]
  9. Fabretti F. , Theilacker C. , Baldassarri L. , Kaczynski Z. , Kropec A. , Holst O. , Huebner J. . ( 2006; ). Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. . Infect Immun 74:, 4164–4171. [CrossRef].[PubMed]
    [Google Scholar]
  10. Fischer W. . ( 1988; ). Physiology of lipoteichoic acids in bacteria. . Adv Microb Physiol 29:, 233–302. [CrossRef] [PubMed]
    [Google Scholar]
  11. Fischer W. , Rösel P. P. . ( 1980; ). The alanine ester substitution of lipoteichoic acid (LTA) in Staphylococcus aureus . . FEBS Lett 119:, 224–226. [CrossRef].[PubMed]
    [Google Scholar]
  12. Fischer W. , Rösel P. , Koch H. U. . ( 1981; ). Effect of alanine ester substitution and other structural features of lipoteichoic acids on their inhibitory activity against autolysins of Staphylococcus aureus . . J Bacteriol 146:, 467–475.[PubMed]
    [Google Scholar]
  13. Fischer W. , Mannsfeld T. , Hagen G. . ( 1990; ). On the basic structure of poly(glycerophosphate) lipoteichoic acids. . Biochem Cell Biol 68:, 33–43. [CrossRef].[PubMed]
    [Google Scholar]
  14. Ganz T. . ( 2001; ). Fatal attraction evaded. How pathogenic bacteria resist cationic polypeptides. . J Exp Med 193:, F31–F34. [CrossRef].[PubMed]
    [Google Scholar]
  15. Gardete S. , Wu S. W. , Gill S. , Tomasz A. . ( 2006; ). Role of VraSR in antibiotic resistance and antibiotic-induced stress response in Staphylococcus aureus . . Antimicrob Agents Chemother 50:, 3424–3434. [CrossRef].[PubMed]
    [Google Scholar]
  16. Gross M. , Cramton S. E. , Götz F. , Peschel A. . ( 2001; ). Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. . Infect Immun 69:, 3423–3426. [CrossRef].[PubMed]
    [Google Scholar]
  17. Haas R. , Koch H. U. , Fischer W. . ( 1984; ). Alanyl turnover from lipoteichoic acid to teichoic acid in Staphylococcus aureus . . FEMS Microbiol Lett 21:, 27–31. [CrossRef]
    [Google Scholar]
  18. Henneke P. , Morath S. , Uematsu S. , Weichert S. , Pfitzenmaier M. , Takeuchi O. , Müller A. , Poyart C. , Akira S. et al. ( 2005; ). Role of lipoteichoic acid in the phagocyte response to group B streptococcus. . J Immunol 174:, 6449–6455.[PubMed] [CrossRef]
    [Google Scholar]
  19. Heptinstall S. , Archibald A. R. , Baddiley J. . ( 1970; ). Teichoic acids and membrane function in bacteria. . Nature 225:, 519–521. [CrossRef].[PubMed]
    [Google Scholar]
  20. Homonylo-McGavin M. K. , Lee S. F. . ( 1996; ). Role of the C terminus in antigen P1 surface localization in Streptococcus mutans and two related cocci. . J Bacteriol 178:, 801–807.[PubMed]
    [Google Scholar]
  21. 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. [CrossRef].[PubMed]
    [Google Scholar]
  22. Jordan S. , Hutchings M. I. , Mascher T. . ( 2008; ). Cell envelope stress response in Gram-positive bacteria. . FEMS Microbiol Rev 32:, 107–146. [CrossRef].[PubMed]
    [Google Scholar]
  23. Kiriukhin M. Y. , Neuhaus F. C. . ( 2001; ). d-Alanylation of lipoteichoic acid: role of the d-alanyl carrier protein in acylation. . J Bacteriol 183:, 2051–2058. [CrossRef].[PubMed]
    [Google Scholar]
  24. Koch H. U. , Döker R. , Fischer W. . ( 1985; ). Maintenance of d-alanine ester substitution of lipoteichoic acid by reesterification in Staphylococcus aureus . . J Bacteriol 164:, 1211–1217.[PubMed]
    [Google Scholar]
  25. Koprivnjak T. , Mlakar V. , Swanson L. , Fournier B. , Peschel A. , Weiss J. P. . ( 2006; ). Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus . . J Bacteriol 188:, 3622–3630. [CrossRef].[PubMed]
    [Google Scholar]
  26. Kristian S. A. , Datta V. , Weidenmaier C. , Kansal R. , Fedtke I. , Peschel A. , Gallo R. L. , Nizet V. . ( 2005; ). d-Alanylation of teichoic acids promotes group A Streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. . J Bacteriol 187:, 6719–6725. [CrossRef].[PubMed]
    [Google Scholar]
  27. 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. [CrossRef].[PubMed]
    [Google Scholar]
  28. Li Y. H. , Lau P. C. , Tang N. , Svensäter G. , Ellen R. P. , Cvitkovitch D. G. . ( 2002; ). Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans . . J Bacteriol 184:, 6333–6342. [CrossRef].[PubMed]
    [Google Scholar]
  29. MacArthur A. E. , Archibald A. R. . ( 1984; ). Effect of culture pH on the d-alanine ester content of lipoteichoic acid in Staphylococcus aureus . . J Bacteriol 160:, 792–793.[PubMed]
    [Google Scholar]
  30. Martínez B. , Zomer A. L. , Rodríguez 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. [CrossRef].[PubMed]
    [Google Scholar]
  31. 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. [CrossRef].[PubMed]
    [Google Scholar]
  32. Mayer M. L. , Phillips C. M. , Stadnyk A. W. , Halperin S. A. , Lee S. F. . ( 2009; ). Synergistic BM-DC activation and immune induction by the oral vaccine vector Streptococcus gordonii and exogenous tumor necrosis factor. . Mol Immunol 46:, 1883–1891. [CrossRef].[PubMed]
    [Google Scholar]
  33. Morath S. , Geyer A. , Hartung T. . ( 2001; ). Structure–function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus . . J Exp Med 193:, 393–398. [CrossRef].[PubMed]
    [Google Scholar]
  34. 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. [CrossRef].[PubMed]
    [Google Scholar]
  35. Perego M. , Glaser P. , Minutello A. , Strauch M. A. , Leopold K. , Fischer W. . ( 1995; ). Incorporation of d-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. . J Biol Chem 270:, 15598–15606.[PubMed] [CrossRef]
    [Google Scholar]
  36. 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. [CrossRef].[PubMed]
    [Google Scholar]
  37. Peterson S. , Cline R. T. , Tettelin H. , Sharov V. , Morrison D. A. . ( 2000; ). Gene expression analysis of the Streptococcus pneumoniae competence regulons by use of DNA microarrays. . J Bacteriol 182:, 6192–6202. [CrossRef].[PubMed]
    [Google Scholar]
  38. Poyart C. , Lamy M. C. , Boumaila C. , Fiedler F. , Trieu-Cuot P. . ( 2001; ). Regulation of d-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. . J Bacteriol 183:, 6324–6334. [CrossRef].[PubMed]
    [Google Scholar]
  39. Poyart C. , Pellegrini E. , Marceau M. , Baptista M. , Jaubert F. , Lamy M. C. , Trieu-Cuot P. . ( 2003; ). Attenuated virulence of Streptococcus agalactiae deficient in d-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. . Mol Microbiol 49:, 1615–1625. [CrossRef].[PubMed]
    [Google Scholar]
  40. Reusch V. M. Jr , Neuhaus F. C. . ( 1971; ). d-Alanine: membrane acceptor ligase from Lactobacillus casei . . J Biol Chem 246:, 6136–6143.[PubMed]
    [Google Scholar]
  41. Spector T. . ( 1978; ). Refinement of the Coomassie blue method of protein quantitation: a simple and linear spectrophotometric assay for ≤0.5 to 50 µg of protein. . Anal Biochem 86:, 142–146. [CrossRef].[PubMed]
    [Google Scholar]
  42. Stipp R. N. , Gonçalves R. B. , Höfling J. F. , Smith D. J. , Mattos-Graner R. O. . ( 2008; ). Transcriptional analysis of gtfB, gtfC, and gbpB and their putative response regulators in several isolates of Streptococcus mutans . . Oral Microbiol Immunol 23:, 466–473. [CrossRef].[PubMed]
    [Google Scholar]
  43. Suntharalingam P. , Senadheera M. D. , Mair R. W. , Lévesque C. M. , Cvitkovitch D. G. . ( 2009; ). The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans . . J Bacteriol 191:, 2973–2984. [CrossRef].[PubMed]
    [Google Scholar]
  44. Syvitski R. T. , Tian X. L. , Sampara K. , Salman A. , Lee S. F. , Jakeman D. L. , Li Y. H. . ( 2007; ). Structure–activity analysis of quorum-sensing signaling peptides from Streptococcus mutans . . J Bacteriol 189:, 1441–1450. [CrossRef].[PubMed]
    [Google Scholar]
  45. Terleckyj B. , Willett N. P. , Shockman G. D. . ( 1975; ). Growth of several cariogenic strains of oral streptococci in a chemically defined medium. . Infect Immun 11:, 649–655.[PubMed]
    [Google Scholar]
  46. Tremblay Y. D. , Lo H. , Li Y. H. , Halperin S. A. , Lee S. F. . ( 2009; ). Expression of the Streptococcus mutans essential two-component regulatory system VicRK is pH and growth-phase dependent and controlled by the LiaFSR three-component regulatory system. . Microbiology 155:, 2856–2865. [CrossRef].[PubMed]
    [Google Scholar]
  47. Weidenmaier C. , Kokai-Kun J. F. , Kristian S. A. , Chanturiya T. , Kalbacher H. , Gross M. , Nicholson G. , Neumeister B. , Mond J. J. , Peschel A. . ( 2004; ). Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. . Nat Med 10:, 243–245. [CrossRef].[PubMed]
    [Google Scholar]
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