Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect

Toxins

Volumn 6, Issue 8, 2014, Pages 2239-2255

  Slamti, Leyla ^a   Perchat, Stéphane ^a   Huillet, Eugénie ^a   Lereclus, Didier ^a  

^a UMR1319 MICALIS   (France)

Author keywords

Adaptation; Bacillus thuringiensis; Cell cell communication; Gene expression; Necrotrophism; RNPP; Sporulation; Virulence

Indexed keywords

BACTERIAL PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; BACILLUS THURINGIENSIS; INSECT; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; QUORUM SENSING;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; INSECTS; QUORUM SENSING; TRANSCRIPTION FACTORS;

EID: 84905576719     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins6082239     Document Type: Review

References (81)

1. Deng, C.; Peng, Q.; Song, F.; Lereclus, D. Regulation of cry gene expression in Bacillus thuringiensis. Toxins 2014, 6, 2194-2209.
2. Sanahuja, G.; Banakar, R.; Twyman, R.M.; Capell, T.; Christou, P. Bacillus thuringiensis: A century of research, development and commercial applications. Plant Biotechnol. J. 2011, 9, 283-300.
3. Sanchis, V. From microbial sprays to insect-resistant transgenic plants: History of the biopesticide Bacillus thuringiensis. A review. Agron. Sustain. Dev. 2011, 31, 217-231.
4. Helgason, E.; Okstad, O.A.; Caugant, D.A.; Johansen, H.A.; Fouet, A.; Mock, M.; Hegna, I.; Kolsto, A.B. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-One species on the basis of genetic evidence. Appl. Environ. Microbiol. 2000, 66, 2627-2630.
5. Stenfors Arnesen, L.P.; Fagerlund, A.; Granum, P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 2008, 32, 579-606.
6. Agata, N.; Mori, M.; Ohta, M.; Suwan, S.; Ohtani, I.; Isobe, M. A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in HEp-2 cells. FEMS Microbiol. Lett. 1994, 121, 31-34.
7. Ehling-Schulz, M.; Svensson, B.; Guinebretiere, M.H.; Lindback, T.; Andersson, M.; Schulz, A.; Fricker, M.; Christiansson, A.; Granum, P.E.; Martlbauer, E.; et al. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 2005, 151, 183-197.
8. Castedo, E.; Castro, A.; Martin, P.; Roda, J.; Montero, C.G. Bacillus cereus prosthetic valve endocarditis. Ann. Thorac. Surg. 1999, 68, 2351-2352.
9. Chu, W.P.; Que, T.L.; Lee, W.K.; Wong, S.N. Meningoencephalitis caused by Bacillus cereus in a neonate. Hong Kong Med. J. 2001, 7, 89-92.
10. Gaur, A.H.; Patrick, C.C.; McCullers, J.A.; Flynn, P.M.; Pearson, T.A.; Razzouk, B.I.; Thompson, S.J.; Shenep, J.L. Bacillus cereus bacteremia and meningitis in immunocompromised children. Clin. Infect. Dis. 2001, 32, 1456-1462.
11. Bottone, E.J. Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 2010, 23, 382-398.
12. Gohar, M.; Faegri, K.; Perchat, S.; Ravnum, S.; Okstad, O.A.; Gominet, M.; Kolsto, A.B.; Lereclus, D. The PlcR virulence regulon of Bacillus cereus. PLoS One 2008, 3, e2793.
13. Salamitou, S.; Ramisse, F.; Brehelin, M.; Bourguet, D.; Gilois, N.; Gominet, M.; Hernandez, E.; Lereclus, D. The PlcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 2000, 146, 2825-2832.
14. Callegan, M.C.; Kane, S.T.; Cochran, D.C.; Gilmore, M.S.; Gominet, M.; Lereclus, D. Relationship of PlcR-regulated factors to Bacillus endophthalmitis virulence. Infect. Immun. 2003, 71, 3116-3124.
15. Dubois, T.; Faegri, K.; Perchat, S.; Lemy, C.; Buisson, C.; Nielsen-LeRoux, C.; Gohar, M.; Jacques, P.; Ramarao, N.; Kolsto, A.B.; et al. Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog. 2012, 8, e1002629.
16. Raymond, B.; Johnston, P.R.; Nielsen-LeRoux, C.; Lereclus, D.; Crickmore, N. Bacillus thuringiensis: An impotent pathogen? Trends Microbiol. 2010, 18, 189-194.
17. Olmedo, G.; Ninfa, E.G.; Stock, J.; Youngman, P. Novel mutations that alter the regulation of sporulation in Bacillus subtilis. Evidence that phosphorylation of regulatory protein SpoOA controls the initiation of sporulation. J. Mol. Biol. 1990, 215, 359-372.
18. Sonenshein, A.L. Control of sporulation initiation in Bacillus subtilis. Curr. Opin. Microbiol. 2000, 3, 561-566.
19. Strauch, M.; Webb, V.; Spiegelman, G.; Hoch, J.A. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc. Natl. Acad. Sci. USA 1990, 87, 1801-1805.
20. Lereclus, D.; Agaisse, H.; Gominet, M.; Chaufaux, J. Overproduction of encapsulated insecticidal crystal proteins in a Bacillus thuringiensis spo0A mutant. Biotechnology (N. Y.) 1995, 13, 67-71.
21. Ng, W.L.; Bassler, B.L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 2009, 43, 197-222.
22. Rutherford, S.T.; Bassler, B.L. Bacterial quorum sensing: Its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2012, 2, doi:10.1101/cshperspect.a012427.
23. Ji, G.; Beavis, R.C.; Novick, R.P. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc. Natl. Acad. Sci. USA 1995, 92, 12055-12059.
24. Novick, R.P.; Geisinger, E. Quorum sensing in Staphylococci. Ann. Rev. Genet. 2008, 42, 541-564.
25. Suzuki, A.; Mori, M.; Sakagami, Y.; Isogai, A.; Fujino, M.; Kitada, C.; Craig, R.A.; Clewell, D.B. Isolation and structure of bacterial sex pheromone, cPD1. Science 1984, 226, 849-850.
26. Kozlowicz, B.K.; Bae, T.; Dunny, G.M. Enterococcus faecalis pheromone-responsive protein PrgX: Genetic separation of positive autoregulatory functions from those involved in negative regulation of conjugative plasmid transfer. Mol. Microbiol. 2004, 54, 520-532.
27. Cook, L.C.; Federle, M.J. Peptide pheromone signaling in Streptococcus and Enterococcus. FEMS Microbiol. Rev. 2014, 38, 473-492.
28. Perego, M.; Hoch, J.A. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 1996, 93, 1549-1553.
29. Lazazzera, B.A.; Solomon, J.M.; Grossman, A.D. An exported peptide functions intracellularly to contribute to cell density signaling in Bacillus subtilis. Cell 1997, 89, 917-925.
30. Perego, M. Forty years in the making: Understanding the molecular mechanism of peptide regulation in bacterial development. PLoS Biol. 2013, 11, e1001516.
31. Shi, K.; Brown, C.K.; Gu, Z.Y.; Kozlowicz, B.K.; Dunny, G.M.; Ohlendorf, D.H.; Earhart, C.A. Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. Proc. Natl. Acad. Sci. USA 2005, 102, 18596-18601.
32. Declerck, N.; Bouillaut, L.; Chaix, D.; Rugani, N.; Slamti, L.; Hoh, F.; Lereclus, D.; Arold, S.T. Structure of PlcR: Insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc. Natl. Acad. Sci. USA 2007, 104, 18490-18495.
33. Baker, M.D.; Neiditch, M.B. Structural basis of response regulator inhibition by a bacterial anti-activator protein. PLoS Biol. 2011, 9, e1001226.
34. Gallego del Sol, F.; Marina, A. Structural basis of Rap phosphatase inhibition by Phr peptides. PLoS Biol. 2013, 11, e1001511.
35. Parashar, V.; Jeffrey, P.D.; Neiditch, M.B. Conformational change-induced repeat domain expansion regulates Rap phosphatase quorum-sensing signal receptors. PLoS Biol. 2013, 11, e1001512.
36. Grenha, R.; Slamti, L.; Nicaise, M.; Refes, Y.; Lereclus, D.; Nessler, S. Structural basis for the activation mechanism of the PlcR virulence regulator by the quorum-sensing signal peptide PapR. Proc. Natl. Acad. Sci. USA 2013, 110, 1047-1052.
37. Zouhir, S.; Perchat, S.; Nicaise, M.; Perez, J.; Guimaraes, B.; Lereclus, D.; Nessler, S. Peptide-binding dependent conformational changes regulate the transcriptional activity of the quorum-sensor NprR. Nucl. Acids Res. 2013, 41, 7920-7933.
38. Lereclus, D.; Agaisse, H.; Gominet, M.; Salamitou, S.; Sanchis, V. 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. 1996, 178, 2749-2756.
39. Agaisse, H.; Gominet, M.; Okstad, O.A.; Kolsto, A.B.; Lereclus, D. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 1999, 32, 1043-1053.
40. Gohar, M.; Okstad, O.A.; Gilois, N.; Sanchis, V.; Kolsto, A.B.; Lereclus, D. Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2002, 2, 784-791.
41. Slamti, L.; Lereclus, D. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 2002, 21, 4550-4559.
42. Bouillaut, L.; Perchat, S.; Arold, S.; Zorrilla, S.; Slamti, L.; Henry, C.; Gohar, M.; Declerck, N.; Lereclus, D. Molecular basis for group-specific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res. 2008, 36, 3791-3801.
43. Pomerantsev, A.P.; Pomerantseva, O.M.; Camp, A.S.; Mukkamala, R.; Goldman, S.; Leppla, S.H. PapR peptide maturation: Role of the NprB protease in Bacillus cereus 569 PlcR/PapR global gene regulation. FEMS Immunol. Med. Microbiol. 2009, 55, 361-377.
44. Gominet, M.; Slamti, L.; Gilois, N.; Rose, M.; Lereclus, D. Oligopeptide permease is required for expression of the Bacillus thuringiensis PlcR regulon and for virulence. Mol. Microbiol. 2001, 40, 963-975.
45. Slamti, L.; Lereclus, D. Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. J. Bacteriol. 2005, 187, 1182-1187.
46. Frenzel, E.; Doll, V.; Pauthner, M.; Lucking, G.; Scherer, S.; Ehling-Schulz, M. CodY orchestrates the expression of virulence determinants in emetic Bacillus cereus by impacting key regulatory circuits. Mol. Microbiol. 2012, 85, 67-88.
47. Lindback, T.; Mols, M.; Basset, C.; Granum, P.E.; Kuipers, O.P.; Kovacs, A.T. CodY, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus. Environ. Microbiol. 2012, 14, 2233-2246.
48. Sonenshein, A.L. CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 2005, 8, 203-207.
49. Stenz, L.; Francois, P.; Whiteson, K.; Wolz, C.; Linder, P.; Schrenzel, J. The CodY pleiotropic repressor controls virulence in gram-positive pathogens. FEMS Immunol. Med. Microbiol. 2011, 62, 123-139.
50. Brillard, J.; Susanna, K.; Michaud, C.; Dargaignaratz, C.; Gohar, M.; Nielsen-Leroux, C.; Ramarao, N.; Kolsto, A.B.; Nguyen-the, C.; Lereclus, D.; et al. The YvfTU two-component system is involved in plcR expression in Bacillus cereus. BMC Microbiol. 2008, 8, 183.
51. Lereclus, D.; Agaisse, H.; Grandvalet, C.; Salamitou, S.; Gominet, M. Regulation of toxin and virulence gene transcription in Bacillus thuringiensis. Int. J. Med. Microbiol. 2000, 290, 295-299.
52. Chitlaru, T.; Gat, O.; Gozlan, Y.; Ariel, N.; Shafferman, A. Differential proteomic analysis of the Bacillus anthracis secretome: Distinct plasmid and chromosome CO2-dependent cross talk mechanisms modulate extracellular proteolytic activities. J. Bacteriol. 2006, 188, 3551-3571.
53. Perchat, S.; Dubois, T.; Zouhir, S.; Gominet, M.; Poncet, S.; Lemy, C.; Aumont-Nicaise, M.; Deutscher, J.; Gohar, M.; Nessler, S.; et al. A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol. Microbiol. 2011, 82, 619-633.
54. Dubois, T.; Perchat, S.; Verplaetse, E.; Gominet, M.; Lemy, C.; Aumont-Nicaise, M.; Grenha, R.; Nessler, S.; Lereclus, D. Activity of the Bacillus thuringiensis NprR-NprX cell-cell communication system is co-ordinated to the physiological stage through a complex transcriptional regulation. Mol. Microbiol. 2013, 88, 48-63.
55. Dubois, T. Etude du système de communication cellulaire-NprX au sein du groupe Bacillus cereus. Ph.D. Thesis, AgroParisTech, Jouy-en-Josas, France, 5 March 2012. (In French)
56. Jiang, M.; Shao, W.; Perego, M.; Hoch, J.A. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 2000, 38, 535-542.
57. Burbulys, D.; Trach, K.A.; Hoch, J.A. Initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay. Cell 1991, 64, 545-552.
58. Perego, M.; Glaser, P.; Hoch, J.A. Aspartyl-phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis. Mol. Microbiol. 1996, 19, 1151-1157.
59. Fujita, M.; Losick, R. 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. 2005, 19, 2236-2244.
60. Core, L.; Perego, M. TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis. Mol. Microbiol. 2003, 49, 1509-1522.
61. Ishikawa, S.; Core, L.; Perego, M. Biochemical characterization of aspartyl phosphate phosphatase interaction with a phosphorylated response regulator and its inhibition by a pentapeptide. J. Biol. Chem. 2002, 277, 20483-20489.
62. Stephenson, S.; Mueller, C.; Jiang, M.; Perego, M. Molecular analysis of Phr peptide processing in Bacillus subtilis. J. Bacteriol. 2003, 185, 4861-4871.
63. Lanigan-Gerdes, S.; Dooley, A.N.; Faull, K.F.; Lazazzera, B.A. Identification of subtilisin, Epr and Vpr as enzymes that produce CSF, an extracellular signalling peptide of Bacillus subtilis. Mol. Microbiol. 2007, 65, 1321-1333.
64. Perego, M. A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc. Natl. Acad. Sci. USA 1997, 94, 8612-8617.
65. Perego, M.; Brannigan, J.A. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 2001, 22, 1541-1547.
66. Mueller, J.P.; Bukusoglu, G.; Sonenshein, A.L. Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: Control of gsiA by the ComP-ComA signal transduction system. J. Bacteriol. 1992, 174, 4361-4373.
67. Molle, V.; Nakaura, Y.; Shivers, R.P.; Yamaguchi, H.; Losick, R.; Fujita, Y.; Sonenshein, A.L. Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J. Bacteriol. 2003, 185, 1911-1922.
68. McQuade, R.S.; Comella, N.; Grossman, A.D. Control of a family of phosphatase regulatory genes (phr) by the alternate sigma factor sigma-H of Bacillus subtilis. J. Bacteriol. 2001, 183, 4905-4909.
69. Stephenson, K.; Hoch, J.A. Evolution of signalling in the sporulation phosphorelay. Mol. Microbiol. 2002, 46, 297-304.
70. Tzeng, Y.L.; Hoch, J.A. Molecular recognition in signal transduction: The interaction surfaces of the Spo0F response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis. J. Mol. Biol. 1997, 272, 200-212.
71. Zapf, J.; Sen, U.; Madhusudan; Hoch, J.A.; Varughese, K.I. A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 2000, 8, 851-862.
72. Brunsing, R.L.; La Clair, C.; Tang, S.; Chiang, C.; Hancock, L.E.; Perego, M.; Hoch, J.A. Characterization of sporulation histidine kinases of Bacillus anthracis. J. Bacteriol. 2005, 187, 6972-6981.
73. Bongiorni, C.; Stoessel, R.; Shoemaker, D.; Perego, M. Rap phosphatase of virulence plasmid pXO1 inhibits Bacillus anthracis sporulation. J. Bacteriol. 2006, 188, 487-498.
74. Petersen, T.N.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8, 785-786.
75. Kall, L.; Krogh, A.; Sonnhammer, E.L. Advantages of combined transmembrane topology and signal peptide prediction-The Phobius web server. Nucl. Acids Res. 2007, 35, W429-W432.
76. Huillet, E.; Tempelaars, M.H.; Andre-Leroux, G.; Wanapaisan, P.; Bridoux, L.; Makhzami, S.; Panbangred, W.; Martin-Verstraete, I.; Abee, T.; Lereclus, D. PlcRa, a new quorum-sensing regulator from Bacillus cereus, plays a role in oxidative stress responses and cysteine metabolism in stationary phase. PLoS One 2012, 7, e51047.
77. Tanous, C.; Soutourina, O.; Raynal, B.; Hullo, M.F.; Mervelet, P.; Gilles, A.M.; Noirot, P.; Danchin, A.; England, P.; Martin-Verstraete, I. The CymR regulator in complex with the enzyme CysK controls cysteine metabolism in Bacillus subtilis. J. Biol. Chem. 2008, 283, 35551-35560.
78. Zuber, P. Management of oxidative stress in Bacillus. Annu. Rev. Microbiol. 2009, 63, 575-597.
79. Mols, M.; Abee, T. Primary and secondary oxidative stress in Bacillus. Environ. Microbiol. 2011, 13, 1387-1394.
80. Newton, G.L.; Rawat, M.; La Clair, J.J.; Jothivasan, V.K.; Budiarto, T.; Hamilton, C.J.; Claiborne, A.; Helmann, J.D.; Fahey, R.C. Bacillithiol is an antioxidant thiol produced in Bacilli. Nat. Chem. Biol. 2009, 5, 625-627.
81. Nicely, N.I.; Parsonage, D.; Paige, C.; Newton, G.L.; Fahey, R.C.; Leonardi, R.; Jackowski, S.; Mallett, T.C.; Claiborne, A. Structure of the type III pantothenate kinase from Bacillus anthracis at 2.0 A resolution: Implications for coenzyme A-dependent redox biology. Biochemistry 2007, 46, 3234-3245.