A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group

Molecular Microbiology

Volumn 82, Issue 3, 2011, Pages 619-633

  Perchat, Stéphane ^a   Dubois, Thomas ^a   Zouhir, Samira ^b   Gominet, Myriam ^c   Poncet, Sandrine ^a   Lemy, Christelle ^a   Aumont Nicaise, Magali ^d   Deutscher, Josef ^a   Gohar, Michel ^a   Nessler, Sylvie ^b   Lereclus, Didier ^a  

^a UMR1319 MICALIS   (France)

^b LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEPTAPEPTIDE; PROTEIN NPRR; PROTEIN NPRX; PROTEINASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; CELL COMMUNICATION; COEVOLUTION; ENZYME SYNTHESIS; GENETIC TRANSCRIPTION; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; NPRA GENE; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SECRETION; SPOROGENESIS; TRANSCRIPTION INITIATION SITE;

BACILLUS CEREUS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL INTERACTIONS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PEPTIDE HYDROLASES; PHYLOGENY; PROMOTER REGIONS, GENETIC; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SPORES, BACTERIAL; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

BACILLUS (BACTERIUM); BACILLUS CEREUS GROUP; BACTERIA (MICROORGANISMS);

EID: 80054845612     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07839.x     Document Type: Article

References (58)

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., and Lereclus, D. (1996) STAB-SD: a Shine-Dalgarno sequence in the 5' untranslated region is a determinant of mRNA stability. Mol Microbiol 20: 633-643.
3. 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.
4. Amrein, K.E., Takacs, B., Stieger, M., Molnos, J., Flint, N.A., and Burn, P. (1995) Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL. Proc Natl Acad Sci USA 92: 1048-1052.
5. Arantes, O., and Lereclus, D. (1991) Construction of cloning vectors for Bacillus thuringiensis. Gene 108: 115-119.
6. Bae, T., Kozlowicz, B.K., and Dunny, G.M. (2004) Characterization of cis-acting prgQ mutants: evidence for two distinct repression mechanisms by Qa RNA and PrgX protein in pheromone-inducible enterococcal plasmid pCF10. Mol Microbiol 51: 271-281.
7. Bouillaut, L., Perchat, S., Arold, S.T., 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.
8. Chitlaru, T., Gat, O., Gozlan, Y., Ariel, N., and Shafferman, A. (2006) Differential proteomic analysis of the Bacillus anthracis secretome: distinct plasmid and chromosome CO2-dependent cross talk mechanisms modulate extracellular proteolytic activities. J Bacteriol 188: 3551-3571.
9. Chung, M.C., Popova, T.G., Millis, B.A., Mukherjee, D.V., Zhou, W., Liotta, L.A., etal. (2006) Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J Biol Chem 281: 31408-31418.
10. Core, L., and Perego, M. (2003) TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis. Mol Microbiol 49: 1509-1522.
11. 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(+) bacteria. Proc Natl Acad Sci USA 104: 18490-18495.
12. Donovan, W.P., Tan, Y., and Slaney, A.C. (1997) Cloning of the nprA gene for neutral protease A of Bacillus thuringiensis and effect of in vivo deletion of nprA on insecticidal crystal protein. Appl Environ Microbiol 63: 2311-2317.
13. 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.
14. Gohar, M., Økstad, O.A., Gilois, N., Sanchis, V., Kolstø, A.-B., and Lereclus, D. (2002) Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2: 784-791.
15. Gohar, M., Gilois, N., Graveline, R., Garreau, C., Sanchis, V., and Lereclus, D. (2005) A comparative study of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis extracellular proteomes. Proteomics 5: 3696-3711.
16. 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.
17. 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.
18. Guérout-Fleury, A.M., Shazand, K., Frandsen, N., and Stragier, P. (1995) Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167: 335-336.
19. Helgason, E., Tourasse, N.J., Meisal, R., Caugant, D.A., and Kolstø, A.B. (2004) Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol 70: 191-201.
20. Hilbert, D.W., and Piggot, P.J. (2004) Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev 68: 234-262.
21. Hill, K.K., Ticknor, L.O., Okinaka, R.T., Asay, M., Blair, H., Bliss, K.A., etal. (2004) Fluorescent amplified fragment length polymorphism analysis of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis isolates. Appl Environ Microbiol 70: 1068-1080.
22. Hoch, J.A. (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3: 165-170.
23. Ivanova, N., Sorokin, A., Anderson, I., Galleron, N., Candelon, B., Kapatral, V., etal. (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423: 87-91.
24. Jiang, M., Grau, R., and Perego, M. (2000) Differential processing of propeptide inhibitors of Rap phosphatases in Bacillus subtilis. J Bacteriol 182: 303-310.
25. Ko, K.S., Kim, J.W., Kim, J.M., Kim, W., Chung, S.I., Kim, I.J., etal. (2004) Population structure of the Bacillus cereus group as determined by sequence analysis of six housekeeping genes and the plcR gene. Infect Immun 72: 5253-5261.
26. 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.
27. Lamb, J.R., Tugendreich, S., and Hieter, P. (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem Sci 20: 257-259.
28. Lanigan-Gerdes, S., Dooley, A.N., Faull, K.F., and Lazazzera, B.A. (2007) Identification of subtilisin, Epr and Vpr as enzymes that produce CSF, an extracellular signalling peptide of Bacillus subtilis. Mol Microbiol 65: 1321-1333.
29. Lapidus, A., Goltsman, E., Auger, S., Galleron, N., Segurens, B., Dossat, C., etal. (2007) Extending the Bacillus cereus group genomics to putative food-borne pathogens of different toxicity. Chem Biol Interact 171: 236-249.
30. Lazazzera, B.A., and Grossman, A.D. (1998) The ins and outs of peptide signaling. Trends Microbiol 6: 288-294.
31. Lecadet, M.M., Blondel, M.O., and Ribier, J. (1980) Generalized transduction in Bacillus thuringiensis var. berliner 1715, using bacteriophage CP54 Ber. J Gen Microbiol 121: 203-212.
32. Leonard, B.A., Podbielski, A., Hedberg, P.J., and Dunny, G.M. (1996) Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc Natl Acad Sci USA 93: 260-264.
33. Lereclus, D., and Arantes, O. (1992) spbA locus ensures the segregational stability of pHT1030, a novel type of Gram-positive replicon. Mol Microbiol 7: 35-46.
34. Lereclus, D., Arantes, O., Chaufaux, J., and Lecadet, M.-M. (1989) Transformation and expression of a cloned ∂-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 60: 211-218.
35. 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.
36. 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.
37. 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.
38. Lövgren, A., Zhang, M., Engström, A., Dalhammar, G., and Landén, R. (1990) Molecular characterization of immune inhibitor A, a secreted virulence protease from Bacillus thuringiensis. Mol Microbiol 4: 2137-2146.
39. Mignot, T., Mock, M., Robichon, D., Landier, A., Lereclus, D., and Fouet, A. (2001) The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis. Mol Microbiol 42: 1189-1198.
40. Moran, C.P. (1993) RNA polymerase and transcription factors. In Bacillus subtilis and Other Gram-Positive Bacteria. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington D.C.: American Society for Microbiology, pp. 653-667.
41. Perego, M., and Brannigan, J.A. (2001) Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22: 1541-1547.
42. Perego, M., and Hoch, J.A. (1996) Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc Natl Acad Sci USA 93: 1549-1553.
43. Perego, M., and Hoch, J.A. (2002) Two component systems, phosphorelays, and regulation of their activities by phosphatases. In Bacillus subtilis and Its Closest Relatives. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington, DC: ASM Press, pp. 473-481.
44. Pottathil, M., and Lazazzera, B.A. (2003) The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 8: 32-45.
45. Ramarao, N., and Lereclus, D. (2005) The InhA1 metalloprotease allows spores of the B. cereus group to escape macrophages. Cell Microbiol 7: 1357-1364.
46. Raymond, B., Johnston, P.R., Nielsen-LeRoux, C., Lereclus, D., and Crickmore, N. (2010) Bacillus thuringiensis: an impotent pathogen? Trends Microbiol 18: 189-194.
47. Rhodius, V.A., and Busby, S.J. (1998) Positive activation of gene expression. Curr Opin Microbiol 1: 152-159.
48. Rocha-Estrada, J., Aceves-Diez, A.E., Guarneros, G., and de la Torre, M. (2010) The RNPP family of quorum-sensing proteins in Gram-positive bacteria. Appl Microbiol Biotechnol 87: 913-923.
49. Shi, K., Brown, C.K., Gu, Z.Y., Kozlowicz, B.K., Dunny, G.M., Ohlendorf, D.H., etal. (2005) Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. Proc Natl Acad Sci USA 102: 18596-18601.
50. 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.
51. 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.
52. Solomon, J.M., Lazazzera, B.A., and Grossman, A.D. (1996) Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. Genes Dev 10: 2014-2024.
53. Stenfors Arnesen, L.P., Fagerlund, A., and Granum, P.E. (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32: 579-606.
54. Stephenson, S., Mueller, C., Jiang, M., and Perego, M. (2003) Molecular analysis of Phr peptide processing in Bacillus subtilis. J Bacteriol 185: 4861-4871.
55. Villafane, R., Bechhofer, D.H., Narayanan, C.S., and Dubnau, D. (1987) Replication control genes of plasmid pE194. J Bacteriol 169: 4822-4829.
56. Waters, C.M., and Bassler, B.L. (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319-346.
57. Wiseman, T., Williston, S., Brandts, J., and Lin, L. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179: 131-137.
58. Yang, H., Sikavi, C., Tran, K., McGillivray, S.M., Nizet, V., Yung, M., etal. (2011) Papillation in Bacillus anthracis colonies: a tool for finding new mutators. Mol Microbiol 79: 1276-1293.