Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain

ISME Journal

Volumn 9, Issue 2, 2015, Pages 286-296

  Deng, Chao ^a,b   Slamti, Leyla ^b   Raymond, Ben ^c   Liu, Guiming ^d   Lemy, Christelle ^b   Gominet, Myriam ^e   Yang, Jingni ^a   Wang, Hengliang ^f   Peng, Qi ^a   Zhang, Jie ^a   Lereclus, Didier ^b   Song, Fuping ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b UMR1319 MICALIS   (France)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^e CNRS   (France)

^f BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS ANTHRACIS; BACILLUS CEREUS; BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); HEXAPODA;

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

BACILLUS THURINGIENSIS; BACTERIAL SPORE; BIOSYNTHESIS; CYTOLOGY; GENETICS; METABOLISM; ORGANISMAL INTERACTION; PHENOTYPE; ULTRASTRUCTURE;

BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; ENDOTOXINS; HEMOLYSIN PROTEINS; MICROBIAL INTERACTIONS; PHENOTYPE; SPORES, BACTERIAL;

EID: 84921552897     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.122     Document Type: Article

References (64)

1. Agaisse H, Lereclus D. (1994 a ). Expression in Bacillus subtilis of the Bacillus thuringiensis cryIIIA toxin gene is not dependent on a sporulation-specific sigma factor and is i ncreased in a spo0A mutant. J Bacteriol 176: 4734-4741.
2. Agaisse H, Lereclus D. (1994 b ). 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.
3. Agaisse H, Lereclus D. (1995). How does Bacillus thuringiensis produce so much insecticidal crystal protein? J Bacteriol 177: 6027-6032.
4. Ag aisse H, Lereclus D. (1996). STAB-SD: a Shine-Dalgarno sequence in the 50 untranslated region is a determinant of mRNA stability. Mol Microbiol 20: 633-643.
5. Bell G. (1985). The origin and early evolution of germ cells as illustrated by the Volvocales. In: Halvorson H, Mornoy A (eds) The Origin and Evolution of Sex. Alan R. Liss: New York, NY, USA, pp 221-256.
6. Berry C. (2012). The bacterium, Lysinibacillus sphaericus, as an insect pathogen. J Invertebr Pathol 109: 1-10.
7. Bizzarri M, Prabhakar A, Bishop A. (2008). Multiple-locus sequence typing analysis of Bacillus thuringiensis recovered from the phylloplane of clover (Trifolium hybridum) in vegetative form. Microb Ecol 55: 619-62 5.
8. Bravo A, Likitvivatanavong S, Gill SS, Soberon M. (2011). Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41: 423-431.
9. Buss LW. (1987). Th e Evolution of Individuality. Princeton University Press: Princeton, NJ, USA.
10. Chao L, Levin BR. (1981). Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA 78: 6324-6328.
11. Chaufaux J, Marchal M, Gilois N, Jehanno I, B uisson C. (1997). Reasearch on natural strains of Bacillus thuringiensis in different biotopes throughout the world. Can J Microbiol 43: 337-343.
12. Du C, Nickerson KW. (1996). Bacillus thuringiensis HD-73 spores have surface-localized Cry1Ac toxin: physiological and pathogenic consequences. Appl Environ Microbiol 62: 3722-3726.
13. Du L, Qiu L, Peng Q, Lereclus D, Zhang J, Song F et al. (2012). Ide ntification of the promoter in the intergenic region between orf1 and cry8Ea1 controlled by sigma H factor. Appl Environ Microbiol 78: 4164-4168.
14. Flardh K, Buttner MJ. (2009). Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
15. Griffin AS, West SA, Buckling A. (2004). Cooperation and competition in pathogenic bacteria. Nature 430: 1024-1027.
16. Guinebretiére M-H, Velge P, Couvert O, Carlin F, Debuyser M-L, Nguyen-The C. (2010). Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (Groups I to VII) rather than spe cies affiliation. J Clin Microbiol 48: 3388-3391.
17. Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, Mock M et al. (2000). Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-on e species on the basis of genetic evidence. Appl Environ Microbiol 66: 2627-2630.
18. Hernandez E,Ramisse F,Ducoureau JP,Cruel T,Cavallo JD. 1998 Bacillus thuringiensis subsp. konkukian (serotype H34) superinfection: case report and experimental evidence of pathogenicity in immunosuppressed mice J Clin Microbiol 36 2138-2139.
19. Hoffmaster AR, Ravel J, Rasko DA, Chapman GD, ChuteMD, Marston CK et al. (2004). Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc Natl Acad Sci USA 101: 8449-8454.
20. Kaiser D, Robinson M, Kroos L. (2010).Myxobacteria, polarity, and multicellular morphogenesis. Cold Spring Harb Perspect Biol 2: a000380.
21. Kho MF, Bellier A, Balasubramani V, Hu Y, Hsu W, Nielsen-LeRoux C et al. (2011). The pore-forming protein Cry5B elicits the pathogenicity of Bacillus sp. against Caenorhabditis elegans. PLoS One 6: e29 122.
22. Kolsto AB, Lereclus D, Mock M. (2002). Genome structure and evolution of the Bacillus cereus group. Curr Top Microbiol Immunol 264: 95-108.
23. Lecadet MM, Blondel MO, Ribier J. (1980). Generalized transduction in Bacillus thuringiensis var. berliner 1715 using bacteriophage CP-54Ber. J Gen Microbiol 121: 203-212.
24. Lereclus D, Arantes O, Chaufaux J, Lecadet M. (1989). Transformation and expression of a cloned deltaendotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 51: 211-217.
25. Liu X,Wang D, Ren J, Tong C, Feng E,Wang X et al. (2013). Identification of the immu nogenic spore and vegetative proteins of Bacillus anthracis vaccine strain A16R. PLoS One 8: e57959.
26. Lopez D, Kolter R. (2010). Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34: 134-149.
27. Lopez D, Vlamakis H, Kolter R. (2009). Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33: 152-163.
28. Losick R, Desplan C. (2008). Stochasticity and cell fate. Science 320: 65-68.
29. Maynard Smith J, Szathmáry E. (1995). The Major Transitions in Evolution. W.H. Freeman Spektrum: Oxford, UK; New York, NY, USA.
30. Michod RE. (1997). Cooperation and conflict in the evolution of individuality .1. Multilevel selection of the organism. Am Nat 149: 607-645.
31. Michod RE. (1999). Darwinian Dynamics : Ev olutionary Transitions in Fitness and Individuality. Princeton University Press: Princeton, NJ, USA; Chichester, UK.
32. Michod RE, Roze D. (2001). Cooperation and conflict in the evolution of multicellularity. Heredity 86: 1-7.
33. Moran Jr CP, Lang N, LeGrice SF, Lee G, Stephens M, Sonenshein AL et al. (1982). Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis. Mol Gen Genet 186: 339-346.
34. Muro-Pastor AM, Hess WR. (2012). Heterocyst differentiation: from single mutants to global approaches. Trends Microbiol 20: 548-557.
35. Ohba M, Mizuki E, Uemori A. (20 09). Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Res 29: 427-433.
36. Perchat S, Dubois T, Zouhir S, Gominet M, Poncet S, Lemy C et al. (2011). A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol Microbiol 82: 619-633.
37. Priest FG, Barker M, Baillie LWJ, Holmes EC, Maiden MCJ. (2004). Population structure and evolution of the Bacillus cereus group. J Bacteriol 186: 7959-7970.
38. Raymond B, Bonsall MB. (2013a). Cooperation and the evolutionary ecology of bacterial virulence: the Bacillus cereus group as a novel study system. Bioessays 35: 706-716.
39. Raymond B, Bonsall MB. (2013b). Co operation and the evolutionary ecology of bacterial virulence: the Bacillus cereus group as a novel study system. BioEssays 35: 706-716.
40. Raymond B,Davis D,Bonsall MB. 2007 Competition and reproduction in mixed infections of pathogenic and non-pathogenic Bacillus spp J Invertebr Pathol 96, 151-155.
41. Raymond B, West SA, Griffin AS, Bonsall MB. (2012). The dynamics of cooperative bacterial virulence in the field. Science 337: 85-88.
42. Raymond B,Wyres KL, Sheppard SK, Ellis RJ, Bonsall MB. (2010a). Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathog 6: e1000905.
43. Raymond B,Wyres KL, Sheppard SK, Ellis RJ, Bonsall MB. (2010b). Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereu s group in the field. PLoS Pathog 6: e1000905.
44. Ross-Gillespie A, Gardner A, West SA, Griffin AS. (2007). Frequency dependence and cooperation: theory and a test with bacteria. Am Nat 170: 331-342.
45. Rossetti V, Schirrmeister BE, Bernasconi MV, Bagheri HC. (2010). The evolutionary path to terminal differentiation and division of labor in cyanobacteria. J Theor Biol 262: 23-34.
46. Sacchi CT,Whitney AM,Mayer LW, Morey R, Steigerwalt A, Boras A et al. (2002). Sequencing of 16S rRNA gene: a rapid tool for identification of Bacillus anthracis. Emerg Infect Dis 8: 1117-1123.
47. San ahuja G, Banakar R, Twyman RM, Capell T, Christou P. (2011). Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J 9: 283-300.
48. Sanchis V, Go har M, Chaufaux J, Arantes O, Meier A, Agaisse H et al. (1999). Development and field performance of a broad-spectrum nonviable asporogenic recombinant strain of Bacillus thuringiensis with greater potency and UV resistance. Appl Environ Microbiol 65: 4032-4039.
49. Sandoz KM, Mitzimberg SM, Schuster M. (2007). Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci USA 104: 15876-15881.
50. Schaeffer P, Millet J, Aubert JP. (1965). Catabolic repression of bacterial sporulation. Proc Natl Acad Sci USA 54: 704-711.
51. Schnepf HE, Lee S, Dojillo J, Burmeister P, Fencil K, Morera L et al. (2005). Characterization of Cry34/Cry35 binary insecticidal proteins from diverse Bacillus thuringiensis strain collections. Appl Environ Microbiol 71: 1765-1774.
52. Shank EA, Kolter R. (2011 ). Extracellular signaling and multicellularity in Bacillus subtilis. Curr Opin Microbiol 14: 741-747.
53. Slamti L, Lereclus D. (2005). Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. J Bacteriol 187: 1182-1187.
54. Sorokin A, Candelon B, Guilloux K, Galleron N, Wackerow-Kouzova N, Ehrlich SD et al. (2006). Multiple-locus sequence typing analysis of Bacillus cereus and Bacillus thuringiensis reveals separate clustering and a distinct population structure of psychrotrophic strains. Appl Environ Microbiol 72: 1569-1578.
55. Stobdan T, Kaur S, Singh A. (2004). Cloning and nucleotide sequence of a novel cry gene from Bacillus thuringiensis. Biotechnol Lett 26: 1153-1156.
56. Strassmann JE, Zhu Y, Queller DC. (2000). Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408: 965-967.
57. Velicer GJ, Kroos L, Lenski RE. (2000). Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404: 598-601.
58. Vilas-Boas GT, Peruca AP, Arantes OM. (2007). Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can J Microbiol 53: 673-687.
59. West SA, Griffin AS, Gardner A. (2007). Evolutionary explanations for cooperation. Curr Biol 17: R661-R672.
60. West SA, Griffin AS, Gardner A, Diggle SP. (2006). Social evolution theory for microorganisms. Nat Rev Microbiol 4: 597-607.
61. Willensdorfer M. (2009). On the evolution of differentiated multicellularity. Evolution 63: 306-323.
62. Yang H,Wang P,Peng Q,Rong R,Liu C,Lereclus D,et al. 2012 Weak transcription of the cry1Ac gene in nonsporulating Bacillus thuringiensis cells Appl Environ Microbiol 78 6466-6474.
63. Yoshisue H, Ihara K, Nishimoto T, Sak ai H, Komano T. (1995). Expression of the genes for insecticidal crystal proteins in Bacillus thuringiensis: cryIVA, not cryIVB, is transcribed by RNA polymerase containing sigma H and that containing sigma E. FEMS Microbiol Lett 12 7: 65-72.
64. Zhu Y, Ji F, Shang H, Zhu Q, Wang P, Xu C et al. (2011). Gene clusters located on two large plasmids determine spore crystal association (SCA) in Bacillus thuringiensis subsp. finitimus strain YBT-020. PLoS One 6: e27164.