1887

Abstract

Most members of the phylum Firmicutes harbour a two-component system (TCS), LiaSR, which is involved in the response to cell envelope stress elicited most notably by inhibitors of the lipid II cycle. In all LiaSR systems studied in detail, LiaSR-mediated signal transduction has been shown to be negatively controlled by a membrane protein, LiaF, encoded upstream of . In this study we have analysed the LiaSR orthologue of (LiaSR). Whole-genome transcriptional profiling indicated that activation of LiaSR results in a remodelling of the cell envelope via the massive upregulation of membrane-associated and extracytoplasmic proteins in the presence of inducing stimuli. As shown for other LiaSR TCSs, LiaSR is activated by cell wall-active antibiotics. We demonstrate that the level of phosphorylated LiaR, which is required for the induction of the LiaSR regulon, is controlled by the interplay between the histidine kinase and phosphatase activities of the bifunctional sensor protein LiaS. Our data suggest that the phosphatase activity of LiaS is stimulated by LiaF in the absence of cell envelope stress.

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2011-02-01
2024-03-29
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References

  1. Alves R., Savageau M. A. 2003; Comparative analysis of prototype two-component systems with either bifunctional or monofunctional sensors: differences in molecular structure and physiological function. Mol Microbiol 48:25–51
    [Google Scholar]
  2. Beier D., Frank R. 2000; Molecular characterization of two-component systems of Helicobacter pylori . J Bacteriol 182:2068–2076
    [Google Scholar]
  3. Belcheva A., Golemi-Kotra D. 2008; A close-up view of the VraSR two-component system. A mediator of Staphylococcus aureus response to cell wall damage. J Biol Chem 283:12354–12364
    [Google Scholar]
  4. Belcheva A., Verma V., Golemi-Kotra D. 2009; DNA-binding activity of the vancomycin resistance associated regulator protein VraR and the role of phosphorylation in transcriptional regulation of the vraSR operon. Biochemistry 48:5592–5601
    [Google Scholar]
  5. Bisicchia P., Noone D., Lioliou E., Howell A., Quigley S., Jensen T., Jarmer H., Devine K. M. 2007; The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis . Mol Microbiol 65:180–200
    [Google Scholar]
  6. Brosius J. 1989; Superpolylinkers in cloning and expression vectors. DNA 8:759–777
    [Google Scholar]
  7. Cotter P. D., Emerson N., Gahan C. G. M., Hill C. 1999; Identification and disruption of lisRK , a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes . J Bacteriol 181:6840–6843
    [Google Scholar]
  8. Cotter P. D., Guinane C. M., Hill C. 2002; The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins. Antimicrob Agents Chemother 46:2784–2790
    [Google Scholar]
  9. Crooks G. E., Hon G., Chandonia J.-M., Brenner S. E. 2004; WebLogo: a sequence logo generator. Genome Res 14:1188–1190
    [Google Scholar]
  10. Dietz P., Gerlach G., Beier D. 2002; Identification of target genes regulated by the two-component system HP166–HP165 of Helicobacter pylori . J Bacteriol 184:350–362
    [Google Scholar]
  11. Eldholm V., Gutt B., Johnsborg O., Brückner R., Maurer P., Hakenbeck R., Mascher T., Havarstein L. S. 2010; The pneumococcal cell envelope stress-sensing system LiaFSR is activated by murein hydrolases and lipid II-interacting antibiotics. J Bacteriol 192:1761–1773
    [Google Scholar]
  12. Fleischer R., Heermann R., Jung K., Hunke S. 2007; Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli . J Biol Chem 282:8583–8593
    [Google Scholar]
  13. Gao R., Stock A. 2009; Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133–154
    [Google Scholar]
  14. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P. other authors 2001; Comparative genomics of Listeria species. Science 294:849–852
    [Google Scholar]
  15. Gueriri I., Cyncynatus C., Dubrac S., Arana A. T., Dussurget O., Msadek T. 2008a; The DegU orphan response regulator of Listeria monocytogenes autorepresses its own synthesis and is required for bacterial motility, virulence and biofilm formation. Microbiology 154:2251–2264
    [Google Scholar]
  16. Gueriri I., Bay S., Dubrac S., Cyncynatus C., Msadek T. 2008b; The Pta–AckA pathway controlling acetyl phosphate levels and the phosphorylation state of the DegU orphan response regulator both play a role in regulating Listeria monocytogenes motility and chemotaxis. Mol Microbiol 70:1342–1357
    [Google Scholar]
  17. Gutu A. D., Wayne K. J., Sham L.-T., Winkler M. E. 2010; Kinetic characterization of the WalRKSpn (VicRK) two-component system of Streptococcus pneumoniae : dependence of WalKSpn (VikK) phosphatase activity on its PAS domain. J Bacteriol 192:2346–2358
    [Google Scholar]
  18. Ho S. N., Hunt H. D., Horton R. M., Pullen J. K., Pease L. R. 1989; Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51–59
    [Google Scholar]
  19. Jiang P., Atkinson M. R., Srisawat C., Sun Q., Ninfa J. A. 2000; Functional dissection of the dimerization and enzymatic activities of Escherichia coli nitrogen regulator II and their regulation by the PII protein. Biochemistry 39:13433–13449
    [Google Scholar]
  20. 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]
  21. Jordan S., Rietkötter E., Strauch M. A., Kalamorz F., Butcher B. G., Helmann J. D., Mascher T. 2007; LiaRS-dependent gene expression is embedded in transition state regulation in Bacillus subtilis . Microbiology 153:2530–2540
    [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
    [Google Scholar]
  23. Kallipolitis B. H., Ingmer H., Gahan C. G., Hill C., Sogaard-Andersen L. 2003; CesRK, a two-component signal transduction system in Listeria monocytogenes , responds to the presence of cell wall-acting antibiotics and affects β -lactam resistance. Antimicrob Agents Chemother 47:3421–3429
    [Google Scholar]
  24. Kamp H. D., Higgins D. E. 2009; Transcriptional and post-transcriptional regulation of the GmaR antirepressor governs temperature-dependent control of flagellar motility in Listeria monocytogenes . Mol Microbiol 74:421–435
    [Google Scholar]
  25. Kramer G., Weiss V. 1999; Functional dissection of the transmitter module of the histidine kinase NtrB in Escherichia coli . Proc Natl Acad Sci U S A 96:604–609
    [Google Scholar]
  26. 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]
  27. Larsen M. H., Kallipolitis B. H., Christiansen J. K., Olsen J. E., Ingmer H. 2006; The response regulator ResD modulates virulence gene expression in response to carbohydrates in Listeria monocytogenes . Mol Microbiol 61:1622–1635
    [Google Scholar]
  28. Laub M. T., Goulian M. 2007; Specificity in two-component signal transduction pathways. Annu Rev Genet 41:121–145
    [Google Scholar]
  29. Mandin P., Fsihi H., Dussurget O., Vergassola M., Milohanic E., Toledo-Arana A., Lasa I., Johansson J., Cossart P. 2005; VirR, a response regulator critical for Listeria monocytogenes virulence. Mol Microbiol 57:1367–1380
    [Google Scholar]
  30. Martínez B., Zomer A. L., Rodriguez 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
    [Google Scholar]
  31. 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]
  32. Mascher T., Zimmer S. L., Smith T.-A., Helmann T. 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]
  33. Mauder N., Williams T., Fritsch F., Kuhn M., Beier D. 2008; Response regulator DegU of Listeria monocytogenes controls temperature-responsive flagellar gene expression in its unphosphorylated state. J Bacteriol 190:4777–4781
    [Google Scholar]
  34. Mohedano M. L., Overweg K., de la Fuente A., Reuter M., Altabe S., Mulholland F., de Mendoza D., López P., Wells J. M. 2005; Evidence that the essential response regulator YycF in Streptococcus pneumoniae modulates expression of fatty acid biosynthesis genes and alters membrane composition. J Bacteriol 187:2357–2367
    [Google Scholar]
  35. Pioszak A. A., Ninfa A. J. 2003; Mechanism of the PII-activated phosphatase activity of Escherichia coli NRII (NtrB): how the different domains of NRII collaborate to act as a phosphatase. Biochemistry 42:8885–8899
    [Google Scholar]
  36. Pioszak A. A., Jiang P., Ninfa A. J. 2000; The Escherichia coli PII signal transduction protein regulates the activities of the two-component system transmitter protein NRII by direct interaction with the kinase domain of the transmitter module. Biochemistry 39:13450–13461
    [Google Scholar]
  37. Riedel C. U., Monk I. R., Casey P. G., Waidmann M. S., Gahan C. G. M., Hill C. 2009; AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes . Mol Microbiol 71:1177–1189
    [Google Scholar]
  38. Rieu A., Weidmann S., Garmyn D., Piveteau P., Guzzo J. 2007; agr system of Listeria monocytogenes EGD-e: role in adherence and differential expression pattern. Appl Environ Microbiol 73:6125–6133
    [Google Scholar]
  39. Rieu A., Briandet R., Habimana O., Garmyn D., Guzzo J., Piveteau P. 2008; Listeria monocytogenes EGD-e biofilms: no mushrooms but a network of knitted chains. Appl Environ Microbiol 74:4491–4497
    [Google Scholar]
  40. Shen A., Kamp H. D., , Gründling A., Higgins D. E. 2006; A bifunctional O -GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev 20:3283–3295
    [Google Scholar]
  41. Sleator R. D., Hill C. 2005; A novel role for the LisRK two-component regulatory system in listerial osmotolerance. Clin Microbiol Infect 11:599–601
    [Google Scholar]
  42. Smyth G. K., Speed T. P. 2003; Normalization of cDNA microarray data. Methods 31:265–273
    [Google Scholar]
  43. Suntharalingam P., Senadheera M. D., Mair R. W., Levesque C. M., Cvitkovitch D. G. 2009; The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans . J Bacteriol 191:2973–2984
    [Google Scholar]
  44. 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]
  45. Szurmant H., Bu L., Brooks C. L. III, Hoch J. A. 2008; An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. Proc Natl Acad Sci U S A 105:5891–5896
    [Google Scholar]
  46. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T. other authors 2009; The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956
    [Google Scholar]
  47. Tremblay Y. D. N., 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
    [Google Scholar]
  48. Vázquez-Boland J. A., Kuhn M., Berche P., Chakraborty T., Domínguez-Bernal G., Goebel W., González-Zorn B., Wehland J., Kreft J. 2001; Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584–640
    [Google Scholar]
  49. Williams T., Bauer S., Beier D., Kuhn M. 2005a; Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect Immun 73:3152–3159
    [Google Scholar]
  50. Williams T., Joseph B., Beier D., Goebel W., Kuhn M. 2005b; Response regulator DegU of Listeria monocytogenes regulates the expression of flagella-specific genes. FEMS Microbiol Lett 252:287–298
    [Google Scholar]
  51. Wolf D., Kalamorz F., Wecke T., Juszczak A., Mäder U., Homuth G., Jordan S., Kirstein J., Hoppert M. other authors 2010; In-depth profiling of the LiaR response of Bacillus subtilis . J Bacteriol 192:4680–4693
    [Google Scholar]
  52. Wuenscher M. D., Köhler S., Goebel W., Chakraborty T. 1991; Gene disruption by plasmid integration in Listeria monocytogenes : insertional inactivation of the listeriolysin determinant lisA . Mol Gen Genet 228:177–182
    [Google Scholar]
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