Activity of the Bacillus thuringiensisNprR-NprX cell-cell communication system is co-ordinated to the physiological stage through a complex transcriptional regulation

Molecular Microbiology

Volumn 88, Issue 1, 2013, Pages 48-63

  Dubois, Thomas ^a,e   Perchat, Stéphane ^a   Verplaetse, Emilie ^a   Gominet, Myriam ^b   Lemy, Christelle ^a   Aumont Nicaise, Magali ^c   Grenha, Rosa ^d   Nessler, Sylvie ^c,d   Lereclus, Didier ^a  

^a UMR1319 MICALIS   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN CODY; PROTEIN PICR; RAP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL GENE; BACTERIAL GROWTH; CELL COMMUNICATION; CELL FUNCTION; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; NPRR GENE; NPRX GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; QUORUM SENSING; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN BINDING;

BACILLUS CEREUS GROUP; BACILLUS THURINGIENSIS; HEXAPODA;

BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION, GENETIC;

EID: 84875628930     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12168     Document Type: Article

References (76)

1. Agaisse, H., and Lereclus, D. (1994) Structural and functional analysis of the promoter region involved in full expression of the cryIIIA toxin gene of Bacillus thuringiensis. Mol Microbiol 13: 97-107.
2. Agaisse, H., Gominet, M., Økstad, O.A., Kolstø, A.B., and Lereclus, D. (1999) PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol Microbiol 32: 1043-1053.
3. Arantes, O., and Lereclus, D. (1991) Construction of cloning vectors for Bacillus thuringiensis. Gene 108: 115-119.
4. Auchtung, J.M., Lee, C.A., and Grossman, A.D. (2006) Modulation of the ComA-dependent quorum response in Bacillus subtilis by multiple Rap proteins and Phr peptides. J Bacteriol 188: 5273-5285.
5. Baldus, J.M., Green, B.D., Youngman, P., and Moran, C.P., Jr (1994) Phosphorylation of Bacillus subtilis transcription factor Spo0A stimulates transcription from the spoIIG promoter by enhancing binding to weak 0A boxes. J Bacteriol 176: 296-306.
6. Bassler, B.L., and Losick, R. (2006) Bacterially speaking. Cell 125: 237-246.
7. Belitsky, B.R., and Sonenshein, A.L. (2008) Genetic and biochemical analysis of CodY-binding sites in Bacillus subtilis. J Bacteriol 190: 1224-1236.
8. Bongiorni, C., Stoessel, R., Shoemaker, D., and Perego, M. (2006) Rap phosphatase of virulence plasmid pXO1 inhibits Bacillus anthracis sporulation. J Bacteriol 188: 487-498.
9. Bouillaut, L., Perchat, S., Arold, S., Zorrilla, S., Slamti, L., Henry, C., etal. (2008) Molecular basis for group-specific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res 36: 3791-3801.
10. Bravo, A., Agaisse, H., Salamitou, S., and Lereclus, D. (1996) Analysis of cryIAa expression in sigE and sigK mutants of Bacillus thuringiensis. Mol Gen Genet 250: 734-741.
11. Bravo, A., Gill, S.S., and Soberon, M. (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49: 423-435.
12. Britton, R.A., Eichenberger, P., Gonzalez-Pastor, J.E., Fawcett, P., Monson, R., Losick, R., and Grossman, A.D. (2002) Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J Bacteriol 184: 4881-4890.
13. Cadot, C., Tran, S.L., Vignaud, M.L., De Buyser, M.L., Kolsto, A.B., Brisabois, A., etal. (2010) InhA1, NprA, and HlyII as candidates for markers to differentiate pathogenic from nonpathogenic Bacillus cereus strains. J Clin Microbiol 48: 1358-1365.
14. Chateau, A., van Schaik, W., Joseph, P., Handke, L.D., McBride, S.M., Smeets, F.M., etal. (2013) Identification of CodY-targets in Bacillus anthracis by genome-wide in vitro binding analysis. J Bacteriol doi:10.1128/JB.02041-12.
15. 2-dependent cross talk mechanisms modulate extracellular proteolytic activities. J Bacteriol 188: 3551-3571.
16. Cosby, W.M., and Zuber, P. (1997) Regulation of Bacillus subtilis sigmaH (spo0H) and AbrB in response to changes in external pH. J Bacteriol 179: 6778-6787.
17. Declerck, N., Bouillaut, L., Chaix, D., Rugani, N., Slamti, L., Hoh, F., etal. (2007) Structure of PlcR: insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc Natl Acad Sci USA 104: 18490-18495.
18. Dixon, L.G., Seredick, S., Richer, M., and Spiegelman, G.B. (2001) Developmental gene expression in Bacillus subtilis crsA47 mutants reveals glucose-activated control of the gene for the minor sigma factor sigma(H). J Bacteriol 183: 4814-4822.
19. Dower, W.J., Miller, J.F., and Ragsdale, C.W. (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16: 6127-6145.
20. Dubois, T., Faegri, K., Perchat, S., Lemy, C., Buisson, C., Nielsen-Leroux, C., etal. (2012) Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog 8: e1002629.
21. Eymann, C., Mittenhuber, G., and Hecker, M. (2001) The stringent response, sigmaH-dependent gene expression and sporulation in Bacillus subtilis. Mol Gen Genet 264: 913-923.
22. Fawcett, P., Eichenberger, P., Losick, R., and Youngman, P. (2000) The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 97: 8063-8068.
23. Frenzel, E., Doll, V., Pauthner, M., Lucking, G., Scherer, S., and Ehling-Schulz, M. (2012) CodY orchestrates the expression of virulence determinants in emetic Bacillus cereus by impacting key regulatory circuits. Mol Microbiol 85: 67-88.
24. Frisby, D., and Zuber, P. (1994) Mutations in pts cause catabolite-resistant sporulation and altered regulation of spo0H in Bacillus subtilis. J Bacteriol 176: 2587-2595.
25. Fujita, M., and Losick, R. (2005) Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev 19: 2236-2244.
26. Fujita, M., and Sadaie, Y. (1998) Feedback loops involving Spo0A and AbrB in in vitro transcription of the genes involved in the initiation of sporulation in Bacillus subtilis. J Biochem (Tokyo) 124: 98-104.
27. Fujita, M., Gonzalez-Pastor, J.E., and Losick, R. (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357-1368.
28. Gibson, J.F., Poole, R.K., Hughes, M.N., and Rees, J.F. (1984) Filamentous growth of Escherichia coli K12 elicited by dimeric, mixed-valence complexes of ruthenium. Arch Microbiol 139: 265-271.
29. Gohar, M., Faegri, K., Perchat, S., Ravnum, S., Økstad, O.A., Gominet, M., etal. (2008) The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3: e2793.
30. Gominet, M., Slamti, L., Gilois, N., Rose, M., and Lereclus, D. (2001) Oligopeptide permease is required for expression of the Bacillus thuringiensis PlcR regulon and for virulence. Mol Microbiol 40: 963-975.
31. Grandvalet, C., Gominet, M., and Lereclus, D. (2001) Identification of genes involved in the activation of the Bacillus thuringiensis inhA metalloprotease gene at the onset of sporulation. Microbiology 147: 1805-1813.
32. Guedon, E., Sperandio, B., Pons, N., Ehrlich, S.D., and Renault, P. (2005) Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151: 3895-3909.
33. Hayashi, K., Kensuke, T., Kobayashi, K., Ogasawara, N., and Ogura, M. (2006) Bacillus subtilis RghR (YvaN) represses rapG and rapH, which encode inhibitors of expression of the srfA operon. Mol Microbiol 59: 1714-1729.
34. Heimpel, A.M., and Angus, T.A. (1959) The site of action of crystalliferous bacteria in Lepidoptera larvae. J Invertebr Pathol 1: 152-170.
35. Helmann, J.D., and Moran, C.P., Jr (2002) RNA polymerase and sigma factors. In Bacillus subtilis and Its Closest Relatives: From Genes to Cells. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington DC: American Society for Microbiology, pp. 289-312.
36. Hense, B.A., Kuttler, C., Muller, J., Rothballer, M., Hartmann, A., and Kreft, J.U. (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5: 230-239.
37. Hilbert, D.W., and Piggot, P.J. (2004) Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev 68: 234-262.
38. Jiang, M., Grau, R., and Perego, M. (2000) Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J Bacteriol 182: 303-310.
39. Kolstø, A.B., Tourasse, N.J., and Økstad, O.A. (2009) What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 63: 451-476.
40. Lazazzera, B.A., Kurtser, I.G., McQuade, R.S., and Grossman, A.D. (1999) An autoregulatory circuit affecting peptide signaling in Bacillus subtilis. J Bacteriol 181: 5193-5200.
41. Lecadet, M.M., Blondel, M.O., and Ribier, J. (1980) Generalized transduction in Bacillus thuringiensis var. berliner 1715 using bacteriophage CP-54Ber. J Gen Microbiol 121: 203-212.
42. Lereclus, D., Arantes, O., Chaufaux, J., and Lecadet, M. (1989) Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 51: 211-217.
43. Lereclus, D., Vallade, M., Chaufaux, J., Arantes, O., and Rambaud, S. (1992) Expansion of insecticidal host range of Bacillus thuringiensis by in vivo genetic recombination. Biotechnology (N Y) 10: 418-421.
44. Lereclus, D., Agaisse, H., Gominet, M., and Chaufaux, J. (1995) Overproduction of encapsulated insecticidal crystal proteins in a Bacillus thuringiensis spo0A mutant. Biotechnology (N Y) 13: 67-71.
45. Lereclus, D., Agaisse, H., Gominet, M., Salamitou, S., and Sanchis, V. (1996) Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J Bacteriol 178: 2749-2756.
46. Lereclus, D., Agaisse, H., Grandvalet, C., Salamitou, S., and Gominet, M. (2000) Regulation of toxin and virulence gene transcription in Bacillus thuringiensis. Int J Med Microbiol 290: 295-299.
47. Lindbäck, T., Mols, M., Basset, C., Granum, P.E., Kuipers, O.P., and Kovacs, A.T. (2012) CodY, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus. Environ Microbiol 14: 2233-2246.
48. Lucking, G., Dommel, M.K., Scherer, S., Fouet, A., and Ehling-Schulz, M. (2009) Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator AbrB, but not by the virulence regulator PlcR. Microbiology 155: 922-931.
49. McQuade, R.S., Comella, N., and Grossman, A.D. (2001) Control of a family of phosphatase regulatory genes (phr) by the alternate sigma factor sigma-H of Bacillus subtilis. J Bacteriol 183: 4905-4909.
50. Molle, V., Nakaura, Y., Shivers, R.P., Yamaguchi, H., Losick, R., Fujita, Y., and Sonenshein, A.L. (2003) Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol 185: 1911-1922.
51. Mueller, J.P., Bukusoglu, G., and Sonenshein, A.L. (1992) Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol 174: 4361-4373.
52. Ogura, M., and Fujita, Y. (2007) Bacillus subtilis rapD, a direct target of transcription repression by RghR, negatively regulates srfA expression. FEMS Microbiol Lett 268: 73-80.
53. Ogura, M., Yamaguchi, H., Yoshida, K., Fujita, Y., and Tanaka, T. (2001) DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B. subtilis two-component regulatory systems. Nucleic Acids Res 29: 3804-3813.
54. Ogura, M., Shimane, K., Asai, K., Ogasawara, N., and Tanaka, T. (2003) Binding of response regulator DegU to the aprE promoter is inhibited by RapG, which is counteracted by extracellular PhrG in Bacillus subtilis. Mol Microbiol 49: 1685-1697.
55. Perchat, S., Dubois, T., Zouhir, S., Gominet, M., Poncet, S., Lemy, C., etal. (2011) A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol Microbiol 82: 619-633.
56. Perego, M., and Brannigan, J.A. (2001) Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22: 1541-1547.
57. Perego, M., Higgins, C.F., Pearce, S.R., Gallagher, M.P., and Hoch, J.A. (1991) The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol 5: 173-185.
58. Perego, M., Glaser, P., and Hoch, J.A. (1996) Aspartyl-phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis. Mol Microbiol 19: 1151-1157.
59. Phillips, Z.E., and Strauch, M.A. (2002) Bacillus subtilis sporulation and stationary phase gene expression. Cell Mol Life Sci 59: 392-402.
60. Pottathil, M., and Lazazzera, B.A. (2003) The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 8: d32-d45.
61. Ratnayake-Lecamwasam, M., Serror, P., Wong, K.W., and Sonenshein, A.L. (2001) Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev 15: 1093-1103.
62. Raymond, B., Johnston, P.R., Nielsen-LeRoux, C., Lereclus, D., and Crickmore, N. (2010) Bacillus thuringiensis: an impotent pathogen? Trends Microbiol 18: 189-194.
63. Rong, S., Rosenkrantz, M.S., and Sonenshein, A.L. (1986) Transcriptional control of the Bacillus subtilis spoIID gene. J Bacteriol 165: 771-779.
64. Rudner, D.Z., LeDeaux, J.R., Ireton, K., and 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 Bacteriol 173: 1388-1398.
65. Salamitou, S., Ramisse, F., Brehelin, M., Bourguet, D., Gilois, N., Gominet, M., etal. (2000) The PlcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146: 2825-2832.
66. Satola, S.W., Baldus, J.M., and Moran, C.P., Jr (1992) Binding of Spo0A stimulates spoIIG promoter activity in Bacillus subtilis. J Bacteriol 174: 1448-1453.
67. van Schaik, W., Chateau, A., Dillies, M.A., Coppee, J.Y., Sonenshein, A.L., and Fouet, A. (2009) The global regulator CodY regulates toxin gene expression in Bacillus anthracis and is required for full virulence. Infect Immun 77: 4437-4445.
68. Schyns, G., Buckner, C.M., and Moran, C.P., Jr (1997) Activation of the Bacillus subtilis spoIIG promoter requires interaction of Spo0A and the sigma subunit of RNA polymerase. J Bacteriol 179: 5605-5608.
69. Slamti, L., and Lereclus, D. (2002) A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 21: 4550-4559.
70. Slamti, L., and Lereclus, D. (2005) Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. J Bacteriol 187: 1182-1187.
71. Sonenshein, A.L. (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8: 203-207.
72. Sonenshein, A.L. (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917-927.
73. Strauch, M., Webb, V., Spiegelman, G., and Hoch, J.A. (1990) The Spo0A protein of Bacillus subtilis is a repressor of the abrB gene. Proc Natl Acad Sci USA 87: 1801-1805.
74. Waters, C.M., and Bassler, B.L. (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319-346.
75. Yang, H., Wang, P., Peng, Q., Rong, R., Liu, C., Lereclus, D., etal. (2012) Weak transcription of the cry1Ac gene in nonsporulating Bacillus thuringiensis cells. Appl Environ Microbiol 78: 6466-6474.
76. Zhang, J., Schairer, H.U., Schnetter, W., Lereclus, D., and Agaisse, H. (1998) Bacillus popilliae cry18Aa operon is transcribed by sigmaE and sigmaK forms of RNA polymerase from a single initiation site. Nucleic Acids Res 26: 1288-1293.