1887

Abstract

The tight control of autolysis by is critical for proper virulence gene expression and biofilm formation. A pair of dicistronic operons, SMU.575/574 () and SMU.1701/1700 (designated ), encode putative membrane proteins that share structural features with the bacteriophage-encoded holin family of proteins, which modulate host cell lysis during lytic infection. Analysis of and mutants revealed a role for these operons in autolysis, biofilm formation, glucosyltransferase expression and oxidative stress tolerance. Expression of was repressed during early exponential phase and was induced over 1000-fold as cells entered late exponential phase, whereas expression declined from early to late exponential phase. A two-component system encoded immediately upstream of (LytST) was required for activation of expression, but not for expression. In addition to availability of oxygen, glucose levels were revealed to affect and transcription differentially and significantly, probably through CcpA (carbon catabolite protein A). Collectively, these findings demonstrate that the Cid/Lrg system can affect several virulence traits of , and its expression is controlled by two major environmental signals, oxygen and glucose. Moreover, / expression is tightly regulated by LytST and CcpA.

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2010-10-01
2024-04-25
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References

  1. Abranches J., Nascimento M. M., Zeng L., Browngardt C. M., Wen Z. T., Rivera M. F., Burne R. A. 2008; CcpA regulates central metabolism and virulence gene expression in Streptococcus mutans. J Bacteriol 190:2340–2349
    [Google Scholar]
  2. Ahn S. J., Burne R. A. 2006; The atlA operon of Streptococcus mutans: role in autolysin maturation and cell surface biogenesis. J Bacteriol 188:6877–6888
    [Google Scholar]
  3. Ahn S. J., Burne R. A. 2007; Effects of oxygen on biofilm formation and the AtlA autolysin of Streptococcus mutans. J Bacteriol 189:6293–6302
    [Google Scholar]
  4. Ahn S. J., Lemos J. A., Burne R. A. 2005; Role of HtrA in growth and competence of Streptococcus mutans UA159. J Bacteriol 187:3028–3038
    [Google Scholar]
  5. Ahn S. J., Wen Z. T., Burne R. A. 2006; Multilevel control of competence development and stress tolerance in Streptococcus mutans UA159. Infect Immun 74:1631–1642
    [Google Scholar]
  6. Ahn S. J., Wen Z. T., Burne R. A. 2007; Effects of oxygen on virulence traits of Streptococcus mutans. J Bacteriol 189:8519–8527
    [Google Scholar]
  7. Ahn S. J., Ahn S. J., Browngardt C. M., Burne R. A. 2009; Changes in biochemical and phenotypic properties of Streptococcus mutans during growth with aeration. Appl Environ Microbiol 75:2517–2527
    [Google Scholar]
  8. Bayles K. W. 2000; The bactericidal action of penicillin: new clues to an unsolved mystery. Trends Microbiol 8:274–278
    [Google Scholar]
  9. Bayles K. W. 2003; Are the molecular strategies that control apoptosis conserved in bacteria?. Trends Microbiol 11:306–311
    [Google Scholar]
  10. Bayles K. W. 2007; The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5:721–726
    [Google Scholar]
  11. Berry A. M., Lock R. A., Hansman D., Paton J. C. 1989; Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect Immun 57:2324–2330
    [Google Scholar]
  12. Blackman S. A., Smith T. J., Foster S. J. 1998; The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144:73–82
    [Google Scholar]
  13. Bowman B. U. Jr, Redmond W. B. 1956; The effects of glucose and of oxygen on autolysis of Mycobacterium tuberculosis. Am Rev Tuberc 73:907–916
    [Google Scholar]
  14. Chandramohan L., Ahn J. S., Weaver K. E., Bayles K. W. 2009; An overlap between the control of programmed cell death in Bacillus anthracis and sporulation. J Bacteriol 191:4103–4110
    [Google Scholar]
  15. Chen Y. Y., Weaver C. A., Mendelsohn D. R., Burne R. A. 1998; Transcriptional regulation of the Streptococcus salivarius 57.I urease operon. J Bacteriol 180:5769–5775
    [Google Scholar]
  16. de Been M., Bart M. J., Abee T., Siezen R. J., Francke C. 2008; The identification of response regulator-specific binding sites reveals new roles of two-component systems in Bacillus cereus and closely related low-GC Gram-positives. Environ Microbiol 10:2796–2809
    [Google Scholar]
  17. Engelberg-Kulka H., Amitai S., Kolodkin-Gal I., Hazan R. 2006; Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135
    [Google Scholar]
  18. Francke C., Kerkhoven R., Wels M., Siezen R. J. 2008; A generic approach to identify transcription Factor-specific operator motifs; inferences for LacI-family mediated regulation in Lactobacillus plantarum WCFS1. BMC Genomics 9:145
    [Google Scholar]
  19. Ghuysen J.-M., Tipper D. J., Strominger J. L. 1966; Enzymes that degrade bacterial cell walls. Methods Enzymol 8:685–699
    [Google Scholar]
  20. Gilpin R. W., Chatterjee A. N., Young F. E. 1972; Autolysis of microbial cells: salt activation of autolytic enzymes in a mutant of Staphylococcus aureus. J Bacteriol 111:272–283
    [Google Scholar]
  21. Groicher K. H., Firek B. A., Fujimoto D. F., Bayles K. W. 2000; The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 182:1794–1801
    [Google Scholar]
  22. Heilmann C., Hussain M., Peters G., Gotz F. 1997; Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24:1013–1024
    [Google Scholar]
  23. Höltje J. V. 1995; From growth to autolysis: the murein hydrolases in Escherichia coli. Arch Microbiol 164:243–254
    [Google Scholar]
  24. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  25. Lau P. C., Sung C. K., Lee J. H., Morrison D. A., Cvitkovitch D. G. 2002; PCR ligation mutagenesis in transformable streptococci: application and efficiency. J Microbiol Methods 49:193–205
    [Google Scholar]
  26. Lewis K. 2000; Programmed death in bacteria. Microbiol Mol Biol Rev 64:503–514
    [Google Scholar]
  27. Loesche W. J. 1986; Role of Streptococcus mutans in human dental decay. Microbiol Rev 50:353–380
    [Google Scholar]
  28. Loo C. Y., Corliss D. A., Ganeshkumar N. 2000; Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol 182:1374–1382
    [Google Scholar]
  29. Mann E. E., Rice K. C., Boles B. R., Endres J. L., Ranjit D., Chandramohan L., Tsang L. H., Smeltzer M. S., Horswill A. R., Bayles K. W. 2009; Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4:e5822
    [Google Scholar]
  30. Mercier C., Durrieu C., Briandet R., Domakova E., Tremblay J., Buist G., Kulakauskas S. 2002; Positive role of peptidoglycan breaks in lactococcal biofilm formation. Mol Microbiol 46:235–243
    [Google Scholar]
  31. Miwa Y., Nakata A., Ogiwara A., Yamamoto M., Fujita Y. 2000; Evaluation and characterization of catabolite-responsive elements ( cre) of Bacillus subtilis. Nucleic Acids Res 28:1206–1210
    [Google Scholar]
  32. Moreno M. S., Schneider B. L., Maile R. R., Weyler W., Saier M. H. Jr 2001; Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol Microbiol 39:1366–1381
    [Google Scholar]
  33. Ochiai T. 1999; Salt-sensitive growth of Staphylococcus aureus: stimulation of salt-induced autolysis by multiple environmental factors. Microbiol Immunol 43:705–709
    [Google Scholar]
  34. Patton T. G., Rice K. C., Foster M. K., Bayles K. W. 2005; The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase. Mol Microbiol 56:1664–1674
    [Google Scholar]
  35. Perkins H. R. 1980 The Bacterial Autolysins London: Chapman & Hall;
    [Google Scholar]
  36. Perry J. A., Cvitkovitch D. G., Levesque C. M. 2009; Cell death in Streptococcus mutans biofilms: a link between CSP and extracellular DNA. FEMS Microbiol Lett 299:261–266
    [Google Scholar]
  37. Qoronfleh M. W., Gustafson J. E., Wilkinson B. J. 1998; Conditions that induce Staphylococcus aureus heat shock proteins also inhibit autolysis. FEMS Microbiol Lett 166:103–107
    [Google Scholar]
  38. Rice K. C., Bayles K. W. 2003; Death's toolbox: examining the molecular components of bacterial programmed cell death. Mol Microbiol 50:729–738
    [Google Scholar]
  39. Rice K. C., Bayles K. W. 2008; Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72:85–109
    [Google Scholar]
  40. Rice K. C., Firek B. A., Nelson J. B., Yang S. J., Patton T. G., Bayles K. W. 2003; The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J Bacteriol 185:2635–2643
    [Google Scholar]
  41. Rice K. C., Nelson J. B., Patton T. G., Yang S. J., Bayles K. W. 2005; Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons. J Bacteriol 187:813–821
    [Google Scholar]
  42. Rice K. C., Mann E. E., Endres J. L., Weiss E. C., Cassat J. E., Smeltzer M. S., Bayles K. W. 2007; The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A 104:8113–8118
    [Google Scholar]
  43. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  44. Shibata Y., Kawada M., Nakano Y., Toyoshima K., Yamashita Y. 2005; Identification and characterization of an autolysin-encoding gene of Streptococcus mutans. Infect Immun 73:3512–3520
    [Google Scholar]
  45. Shockman G. D., Holfje J.-V. 1994 Microbial Peptidoglycan (Murein) Hydrolases Amsterdam: Elsevier;
    [Google Scholar]
  46. Smith T. J., Blackman S. A., Foster S. J. 2000; Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249–262
    [Google Scholar]
  47. Sofia H. J., Chen G., Hetzler B. G., Reyes-Spindola J. F., Miller N. E. 2001; Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res 29:1097–1106
    [Google Scholar]
  48. Sturges W. S., Rettger L. F. 1922; Bacterial autolysis. J Bacteriol 7:551–577
    [Google Scholar]
  49. Tobin P. J., Mani N., Jayaswal R. K. 1994; Effect of physiological conditions on the autolysis of Staphylococcus aureus strains. Antonie van Leeuwenhoek 65:71–78
    [Google Scholar]
  50. Wang I. N., Smith D. L., Young R. 2000; Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54:799–825
    [Google Scholar]
  51. Ward J. B., Williamson R. 1984 Bacterial Autolysins: Specificity and Function Amsterdam: Elsevier;
    [Google Scholar]
  52. Wells J. E., Russell J. B. 1996; The effect of growth and starvation on the lysis of the ruminal cellulolytic bacterium Fibrobacter succinogenes. Appl Environ Microbiol 62:1342–1346
    [Google Scholar]
  53. Wen Z. T., Burne R. A. 2002; Analysis of cis- and trans-acting factors involved in regulation of the Streptococcus mutans fructanase gene ( fruA. J Bacteriol 184:126–133
    [Google Scholar]
  54. Wuenscher M. D., Kohler S., Bubert A., Gerike U., Goebel W. 1993; The iap gene of Listeria monocytogenes is essential for cell viability, and its gene product, p60, has bacteriolytic activity. J Bacteriol 175:3491–3501
    [Google Scholar]
  55. Wunder D., Bowen W. H. 2000; Effects of antibodies to glucosyltransferase on soluble and insolubilized enzymes. Oral Dis 6:289–296
    [Google Scholar]
  56. Yabu K., Kaneda S. 1995; Salt-induced cell lysis of Staphylococcus aureus. Curr Microbiol 30:299–303
    [Google Scholar]
  57. Yamashita Y., Bowen W. H., Burne R. A., Kuramitsu H. K. 1993; Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infect Immun 61:3811–3817
    [Google Scholar]
  58. Yarmolinsky M. B. 1995; Programmed cell death in bacterial populations. Science 267:836–837
    [Google Scholar]
  59. Young R. 1992; Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56:430–481
    [Google Scholar]
  60. Young R. 2002; Bacteriophage holins: deadly diversity. J Mol Microbiol Biotechnol 4:21–36
    [Google Scholar]
  61. Young R., Blasi U. 1995; Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev 17:191–205
    [Google Scholar]
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