1887

Abstract

uses two-component signal transduction systems to sense intra- and extracellular stimuli to adapt to fluctuating environmental situations. Regulator aspartate phosphatases (Raps) have important roles in these processes, as they can dephosphorylate certain response-regulators, and are themselves subject to cell-density-controlled inhibition by secreted Phr (phosphate regulator) peptides. Eleven chromosomal genes encode this family of phosphatases, but in addition, certain strains contain endogenous plasmids with genes for homologous Rap–Phr systems. Plasmid pTA1060 encodes Rap60 and its antagonistic signalling molecule Phr60. Strikingly, expression of Rap60 in 168 strongly repressed the production of proteolytic enzymes. In fact, the transcription of the gene, encoding a major extracellular protease, was shown to be decreased upon Rap60 expression, whereas this effect could be antagonized by the extracellular addition of synthetic Phr60 pentapeptide. Finally, transcription studies suggest that Rap60 dephosphorylates a component of the phosphorelay and is coupled to transcription by the transition-state regulator AbrB. In conclusion, these data show that endogenous plasmids contain functional Rap–Phr systems and for the first time, that Rap–Phr systems can mediate cell-density controlled production of secreted proteases. This quorum-sensing mechanism might enable to suppress protease production under conditions of low cell densities when nutrients are still available in sufficient amounts.

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2003-01-01
2020-04-04
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References

  1. Birrer G. A, Cromwick A. M., Gross R. A. 1994; Gamma-poly- (glutamic acid) formation by Bacillus licheniformis physiological and biochemical studies. Int J Biol Macromol16:265–275
    [Google Scholar]
  2. Bolhuis A, Koetje E, Dubois J. Y, Vehmaanpera J, Venema G, Bron S., van Dijl J. M. 2000; Did the mitochondrial processing peptidase evolve from a eubacterial regulator of gene expression?. Mol Biol Evol17:198–201
    [Google Scholar]
  3. Bron S., Venema G. 1972; Ultraviolet interaction and excision repair in Bacillus subtilis . I. Construction and characterization of a transformable eightfold auxotrophic strain and two ultraviolet-sensitive derivatives. Mutat Res15:1–10
    [Google Scholar]
  4. Dahl M. K, Msadek T, Kunst F., Rapoport G. 1992; The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis. J Biol Chem267:14509–14514
    [Google Scholar]
  5. Dubnau D. 1991; Genetic competence in B. subtilis. Microbiol Rev55:395–424
    [Google Scholar]
  6. Fabret C, Feher V. A., Hoch J. A. 1999; Two-component signal transduction in Bacillus subtilis : how one organism sees its world. J Bacteriol181:1975–1983
    [Google Scholar]
  7. Ferrari E, Henner D. J, Perego M., Hoch J. A. 1988; Transcription of Bacillus subtilis subtilisin and expression of subtilisin in sporulation mutants. J Bacteriol170:289–295
    [Google Scholar]
  8. Gray K. M. 1997; Intercellular communication and group behavior in bacteria. Trends Microbiol5:184–188
    [Google Scholar]
  9. Grossman A. D. 1995; Genetic networks controlling the initiation of sporulation and the development of competence in Bacillus subtilis. Annu Rev Genet29:477–508
    [Google Scholar]
  10. Hoch J. A. 1993; The phosphorelay signal transduction pathway in the initiation of Bacillus subtilis sporulation. J Cell Biochem51:55–61
    [Google Scholar]
  11. Jiang M, Grau R., Perego M. 2000a; Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J Bacteriol182:303–310
    [Google Scholar]
  12. Jiang M, Shao W, Perego M., Hoch J. A. 2000b; Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol38:535–542
    [Google Scholar]
  13. Kallio P. T, Fagelson J. E, Hoch J. A., Straugh M. A. 1991; The transition state regulator Hpr of Bacillus subtilis is a DNA-binding protein. J Biol Chem266:13411–13417
    [Google Scholar]
  14. Kim L, Mogk A., Schumann W. 1996; A xylose-inducible Bacillus subtilis integration vector and its application. Gene181:71–76
    [Google Scholar]
  15. Kunst F., Rapoport G. 1995; Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol77:2403–2407
    [Google Scholar]
  16. Kunst F, Msadek T, Bignon J., Rapoport G. 1994; The DegS/DegU and ComP/ComA two-component systems are part of a network controlling degradative enzyme synthesis and competence in Bacillus subtilis. Res Microbiol145:393–402
    [Google Scholar]
  17. Kunst F, Ogasawara N, Moszer. 148 other authors 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature390:249–256
    [Google Scholar]
  18. Lazazzera B. A, Solomon J. M., Grossman A. D. 1997; An exported peptide functions intracellularly to contribute to cell density signalling in B. subtilis. Cell89:917–925
    [Google Scholar]
  19. Lazazzera B. A, Kurtser I. G, McQuade R. S., Grossman A. L. 1999; An autoregulatory circuit affecting peptide signaling in Bacillus subtilis. J Bacteriol181:5193–5200
    [Google Scholar]
  20. Marahiel M. A, Nakano M. M., Zuber P. 1993; Regulation of peptide antibiotic production in Bacillus. Mol Microbiol7:631–636
    [Google Scholar]
  21. Meijer W. J. J, Wisman B. A, Terpstra P, Thorsted P. B, Thomas C. M, Holsappel S, Venema G., Bron S. 1998; Rolling-circle plasmids from Bacillus subtilis : complete nucleotide sequences and analyses of genes of pTA1015, pTA1040, pTA1050 and pTA1060, and comparisons with related plasmids from Gram-positive bacteria. FEMS Microbiol Lett37:283–288
    [Google Scholar]
  22. Miller J. H. 1982; Experiments in Molecular Genetics Cold Spring Harbor, New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  23. Msadek T, Kunst F, Henner D, Klier A, Rapoport G., Dedonder R. 1990; Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis : expression of the regulatory genes and analysis of mutations in DegS and DegU. J Bacteriol172:824–834
    [Google Scholar]
  24. Msadek T, Kunst F, Henner D, Klier A., Rapoport G. 1991; DegS-DegU and ComP-ComA modulator-effector pairs control expression of the Bacillus subtilis pleiotropic regulatory gene degQ. J Bacteriol173:2366–2377
    [Google Scholar]
  25. Mueller J. P, Bukusoglu G., Sonenshein A. L. 1992; Transcriptional regulation of Bacillus subtilis glucose starvation inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol174:4361–4373
    [Google Scholar]
  26. Nagai T, Phan Tran L. S, Inatsu Y., Itoh Y. 2000; A new IS 4 family insertion sequence, IS4Bsu1, responsible for genetic instability of poly-gamma-glutamic acid production in Bacillus subtilis. J Bacteriol182:2387–2392
    [Google Scholar]
  27. Nakano M. M, Xia L., Zuber P. 1991; Transcription initiation region of the srfA operon, which is controlled by the comP-comA signal transduction system in Bacillus subtilis. J Bacteriol173:5487–5493
    [Google Scholar]
  28. Perego M. 1997; A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc Natl Acad Sci U S A94:8612–8617
    [Google Scholar]
  29. Perego M. 1998; Kinase-phosphatase competition regulates Bacillus subtilis development. Trends Microbiol6:366–370
    [Google Scholar]
  30. Perego M, Higgins C. F, Pearce S. R, Gallagher M. P., Hoch J. A. 1991; The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol5:173–185
    [Google Scholar]
  31. Perego M, Hanstein C, Welsh K. M, Djavakhishvili T, Glaser P., Hoch J. A. 1994; Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell76:1047–1055
    [Google Scholar]
  32. Perego M, Glaser P., Hoch J. A. 1996; Aspartyl-phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis. Mol Microbiol19:1151–1170
    [Google Scholar]
  33. Priest F. G. 1993; Systematics and ecology of Bacillus . In Bacillus subtilis and Other Gram-Positive Bacteria pp3–16 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  34. Roggiani M., Dubnau D. 1993; ComA, a phosphorylated response regulator protein of Bacillus subtilis , binds to the promoter region of srfA. J Bacteriol175:3182–3187
    [Google Scholar]
  35. Rudner D. Z, Ledeaux J. R, Ireton K., Grossman A. D. 1991; The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J Bacteriol173:1388–1398
    [Google Scholar]
  36. Sambrook J, Fritsch E. F., Maniatis T. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor; New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  37. Schaeffer P, Millet J., Aubert P. J. 1965; Catabolic repression of bacterial sporulation. Proc Natl Acad Sci U S A54:704–711
    [Google Scholar]
  38. Schumann W, Ehrlich D., Ogasawara N. 2000; Functional Analysis of Bacterial Genes: a Practical Manual New York: Wiley;
    [Google Scholar]
  39. Smith I. 1993; Regulatory proteins that control late-growth development. In Bacillus subtilis and Other Gram-Positive Bacteria pp785–800 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  40. Solomon J. M, Lazazzera B. A., Grossman A. D. 1996; Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. Genes Dev10:2014–2024
    [Google Scholar]
  41. Steinmetz M., Richter R. 1994; Plasmids designed to alter the antibiotic resistance expressed by insertion mutations in Bacillus subtilis , through in vivo recombination. Gene142:79–83
    [Google Scholar]
  42. Strauch M. A., Hoch J. A. 1993; Transcription-state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol Microbiol7:337–342
    [Google Scholar]
  43. Tjalsma H, Noback M. A, Bron S, Venema G, Yamane K., van Dijl J. M. 1997; Bacillus subtilis contains four closely related type I signal peptidases with overlapping substrate specificities: constitutive and temporally controlled expression of different sip genes. J Biol Chem272:25983–25992
    [Google Scholar]
  44. Tjalsma H, Bolhuis A, van Roosmalen M. L. 7 other authors 1998; Functional analysis of the secretory precursor processing machinery of Bacillus subtilis : identification of a eubacterial homologue of archaeal and eukaryotic signal peptidases. Genes Dev12:2318–2331
    [Google Scholar]
  45. Tjalsma H, van den Dolder J, Meijer W. J. J, Venema G, Bron S., van Dijl J. M. 1999; The plasmid-encoded type I signal peptidase SipP can functionally replace the major signal peptidases SipS and SipT of Bacillus subtilis. J Bacteriol181:2448–2454
    [Google Scholar]
  46. Tjalsma H, Bolhuis A, Jongbloed J. D, Bron S., van Dijl J. M. 2000; Signal peptide-dependent protein transport in Bacillus subtilis : a genome-based survey of the secretome. Microbiol Mol Biol Rev64:515–547
    [Google Scholar]
  47. Trach K, Burbulys D, Strauch M.. 7 other authors 1991; Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay. Res Microbiol142:815–823
    [Google Scholar]
  48. Tzeng Y. L, Feher V. A, Cavanagh J, Perego M., Hoch J. A. 1998; Characterization of interactions between a two-component response regulator, and its phosphatase, RapB. Biochemistry37:16538–16545
    [Google Scholar]
  49. Uozumi T, Ozaki A, Beppu T., Arima K. 1980; New cryptic plasmid of Bacillus subtilis and restriction analysis of other plasmids found by general screening. J Bacteriol142:315–318
    [Google Scholar]
  50. Vagner V, Dervyn E., Ehrlich S. D. 1998; A vector for systematic gene inactivation in B. subtilis. Microbiology144:3097–3104
    [Google Scholar]
  51. Yang M, Ferrari E, Chen E., Henner J. 1986; Identification of the pleiotropic sacQ gene of Bacillus subtilis. J Bacteriol166:113–119
    [Google Scholar]
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