Characterization of a novel Cry9Bb δ-endotoxin from Bacillus thuringiensis

Journal of Invertebrate Pathology

Volumn 98, Issue 3, 2008, Pages 320-328

  Silva Werneck, J O ^a   Ellar, D J ^b  

^a EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Anticarsia gemmatalis; Bacillus thuringiensis; Biological control; Characterization; Cry toxins; cry9 gene; Manduca sexta

Indexed keywords

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

ANIMAL; ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL GENE; BIOLOGICAL PEST CONTROL; CHEMISTRY; GENETICS; LARVA; LEPIDOPTERA; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; PATHOGENICITY; SEQUENCE ANALYSIS;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; CLONING, MOLECULAR; ENDOTOXINS; GENES, BACTERIAL; HEMOLYSIN PROTEINS; INSECTICIDES; LARVA; MANDUCA; PEST CONTROL, BIOLOGICAL; SEQUENCE ANALYSIS, PROTEIN;

ANTICARSIA GEMMATALIS; BACILLUS THURINGIENSIS; BACILLUS THURINGIENSIS SEROVAR JAPONENSIS; MANDUCA SEXTA; MUCUNA;

EID: 45849086558     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2008.03.012     Document Type: Article

References (74)

1. Accelrys, Wisconsin Package, version 10.3, San Diego, CA.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
3. Asano S. Identification of cry gene from Bacillus thuringiensis by PCR and isolation of unique insecticidal bacteria. Mem. Fac. Agric. Hokkaido Uni. 19 (1996) 529-563
4. Bell R.A., and Joachim F.G. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann. Entomol. Soc. Am. 69 (1976) 365-373
5. Ben-Dov E., Wang Q., Zaritsky A., Manasherob R., Barak Z., Schneider B., Khamraev A., Baizhanov M., Glupov V., and Margalith Y. Multiplex PCR screening to detect cry9 genes in Bacillus thuringiensis strains. Appl. Environ. Microbiol. 65 (1999) 3714-3716
6. Birnboin H.C., and Doly J.A. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7 (1979) 1513-1523
7. Bone E.J., and Ellar D.J. Transformation of Bacillus thuringiensis by electroporation. FEMS Microbiol. Lett. 58 (1989) 171-178
8. Bravo A. Phylogenetic relationships of Bacillus thuringiensis delta-endotoxin family proteins and their functional domains. J. Bacteriol. 179 (1997) 2793-2801
9. Bravo A., Sarabia S., Lopez L., Ontiveros H., Abarca C., Ortiz A., Ortiz M., Lina L., Villalobos F.J., Peña G., Nuñez-Valdez M.E., Soberón M., and Quintero R. Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection. Appl. Environ. Microbiol. 64 (1998) 4965-4972
10. Cerón J., Covarrubias L., Quintero R., Ortíz A., Ortíz M., Aranda E., Lina L., and Bravo A. PCR analysis of the cryI insecticidal crystal family genes from Bacillus thuringiensis. Appl. Environ. Microbiol. 60 (1994) 353-356
11. Cerón J., Ortíz A., Quintero R., Guereca L., and Bravo A. Specific PCR primers directed to identify cryI and cryIII genes within a Bacillus thuringiensis strain collection. Appl. Environ. Microbiol. 61 (1995) 3826-3831
12. Choi S.K., Shin B.S., Kong E.M., Rho H.M., and Park S.H. Cloning of a new Bacillus thuringiensis cry1I-type crystal protein gene. Curr. Microbiol. 41 (2000) 65-69
13. Crickmore N., and Ellar D.J. Involvement of a possible chaperonin in the efficient expression of a cloned CryIIA δ-endotoxin gene in Bacillus thuringiensis. Mol. Microbiol. 6 (1992) 1533-1537
14. Crickmore N., Nicholls C., Earp D.J., Hodgman T.C., and Ellar D.J. The construction of Bacillus thuringiensis strains expressing novel entomocidal delta-endotoxin combinations. Biochem. J. 270 (1990) 133-136
15. de Maagd R.A., Bravo A., Berry C., Crickmore N., and Schnepf H.E. Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu. Rev. Genet. 37 (2003) 409-433
16. de Maagd R.A., Bravo A., and Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. 17 (2001) 193-199
17. De-Souza M.T., Lima M.I., Silva-Werneck J.O., and Dias J.M.C.S. Ultrastructural and molecular characterization of the parasporal crystal proteins of Bacillus thuringiensis subsp. kurstaki S93 active against Spodoptera frugiperda. Biocell 23 (1999) 43-49
18. Edwards, D.L., Payne, J., Soares, G.G., 1990. Novel Isolates of Bacillus thuringiensis Having Activity Against Nematodes. US Patent 4,948,734.
19. Espinasse S., Chaufaux J., Buisson C., Perchat S., Gohar M., Bourguet D., and Sanchis V. Occurrence and linkage between secreted insecticidal toxins in natural isolates of Bacillus thuringiensis. Curr. Microbiol. 47 (2003) 501-507
20. Estruch J.J., Carozzi N.B., Desai N., Duck N.B., Warren G.W., and Koziel M.G. Transgenic plants: an emerging approach to pest control. Nat. Biotechnol. 15 (1997) 137-141
21. Estruch J.J., Warren G.W., Mullins M.A., Nye G.J., Craig J.A., and Koziel M.G. Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc. Natl. Acad. Sci. USA 93 (1996) 5389-5394
22. Feitelson J.S., Payne J., and Kim L. Bacillus thuringiensis: insects and beyond. Bio/Technology 10 (1992) 271-275
23. Finney D.J. Probit Analysis (1971), Cambridge University Press, Cambridge, UK
24. Gerber D., and Shai Y. Insertion and organization within membranes of the delta-endotoxin pore-forming domain, helix 4-loop-helix 5, and inhibition of its activity by a mutant helix 4 peptide. J. Biol. Chem. 275 (2000) 23602-23607
25. Gilliland A., Chambers C.E., Bone E.J., and Ellar D.J. Role of Bacillus thuringiensis Cry1 δ endotoxin binding in determining potency during lepidopteran larval development. Appl. Environ. Microbiol. 68 (2002) 1509-1515
26. Gleave A.P., Williams R., and Hedges R.J. Screening by polymerase chain reaction of Bacillus thuringiensis serotypes for the presence of cryV-like insecticidal protein genes and characterization of a cryV gene cloned from B. thuringiensis subsp. kurstaki. Appl. Environ. Microbiol. 59 (1993) 1683-1687
27. Hinks, D.A., 1998. Molecular Analysis of a Bacillus thuringiensis Strain Toxic to Ceratitis capitata. Ph.D. Thesis, Department of Biochemistry. University of Cambridge, Cambridge.
28. Höfte H., and Whiteley H.R. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53 (1989) 242-255
29. Ibarra J.E., del Rincon M.C., Orduz S., Noriega D., Benintende G., Monnerat R., Regis L., de Oliveira C.M., Lanz H., Rodriguez M.H., Sanchez J., Pena G., and Bravo A. Diversity of Bacillus thuringiensis strains from Latin America with insecticidal activity against different mosquito species. Appl. Environ. Microbiol. 69 (2003) 5269-5274
30. Iizuka, T., Sasaki, J., Asano, S., Yamamoto, T., Screening and cloning of novel toxin genes from Bacillus thuringiensis strains encoding a highly scarabecidal protein. In: SIP (Ed.), 29th Annual Meeting of the SIP and Third International Colloquium on Bacillus thuringiensis, Cordoba, Spain, 1996, p. 38.
31. Kostichka K., Warren G.W., Mullins M., Mullins A.D., Palekar N.V., Craig J.A., Koziel M.G., and Estruch J.J. Cloning of a cryV-type insecticidal protein gene from Bacillus thuringiensis: the cryV-encoded protein is expressed early in stationary phase. J. Bacteriol. 178 (1996) 2141-2144
32. Kotze A.C., O'Grady J., Gough J.M., Pearson R., Bagnall N.H., Kemp D.H., and Akhurst R.J. Toxicity of Bacillus thuringiensis to parasitic and free-living life-stages of nematode parasites of livestock. Int. J. Parasitol. 35 (2005) 1013-1022
33. Krieg A., and Langenbruch G.A. Susceptibility of arthropod species to Bacillus thuringiensis. In: Burges H.D. (Ed). Microbial Control of Pests and Plant Diseases 1970-1980 (1981), Academic Press, London 837-896
34. Laemmli U.K., and Favre M. Maturation of the head of bacteriophage T4. J. Mol. Biol. 80 (1973) 575-599
35. Lambert B., Buysse L., Decock C., Jansens S., Piens C., Saey B., Seurinck J., Van Audenhove K., Van Rie J., Van Vliet A., and Peferoen M. A Bacillus thuringiensis insecticidal crystal protein with a high activity against members of the family Noctuidae. Appl. Environ. Microbiol. 62 (1996) 80-86
36. Lee M.K., Jenkins J.L., You T.H., Curtiss A., Son J.J., Adang M.J., and Dean D.H. Mutations at the arginine residues in alpha-8 loop of Bacillus thuringiensis delta-endotoxin Cry1Ac affect toxicity and binding to Manduca sexta and Lymantria dispar aminopeptidase N. FEBS Lett. 497 (2001) 108-112
37. Lightwood, D.J., 1999. Potency Determinants of the Bacillus thuringiensis δ-endotoxins. Ph.D. Thesis, Department of Biochemistry, University of Cambridge, Cambridge.
38. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
39. Martínez C., and Caballero P. Contents of cry genes and insecticidal toxicity of Bacillus thuringiensis strains from terrestrial and aquatic habitats. J. Appl. Microbiol. 92 (2002) 745-752
40. Masson L., Erlandson M., Puzstai-Carey M., Brousseau R., Juárez-Pérez V., and Frutos R. A holistic approach for determining the entomopathogenic potential of Bacillus thuringiensis strains. Appl. Environ. Microbiol. 64 (1998) 4782-4788
41. Midoh, N., Oyama, K., 1998. Bacillus thuringiensis cry Gene for Insecticidal Crystal Protein. Unpublished work. Available from: www.ncbi.nlm.nih.gov.
42. Monnerat R.G., Batista A.C., Medeiros P.T., Martins E.S., Melatti V.M., Praça L.B., Dumas V.F., Morinaga C., Demo C., Gomes A.C.M., Falcão R., Siqueira C.B., Silva-Werneck J.O., and Berry C. Screening of Brazilian Bacillus thuringiensis isolates active against Spodoptera frugiperda, Plutella xylostella and Anticarsia gemmatalis. Biol. Control. 41 (2007) 291-295
43. Payne, J., Cannon, R.J.C., Ralph, A.L., 1994. Bacillus thuringiensis Isolates for Controlling Acarides. US Patent 5,350,576.
44. Pigott C.R., and Ellar D.J. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71 (2007) 255-281
45. Porcar M., and Juárez-Pérez V. PCR-based identification of Bacillus thuringiensis pesticidal crystal genes. FEMS Microbiol. Rev. 26 (2003) 419-432
46. Pospiesch A., and Neumann B. A versatile quick-prep of genomic DNA from Gram-positive bacteria. Trends Genet. 11 (1995) 217-218
47. Romeis J., Meissle M., and Bigler F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24 (2006) 63-71
48. Ruiu L., Delrio G., Ellar D.J., Floris I., Paglietti B., Rubino S., and Satta A. Lethal and sublethal effects of Brevibacillus laterosporus on the housefly (Musca domestica). Entomol. Exper. Appl. 118 (2006) 137-144
49. Ruiz de Escudero I., Estela A., Porcar M., Martinez C., Oguiza J.A., Escriche B., Ferre J., and Caballero P. Molecular and insecticidal characterization of a Cry1I protein toxic to insects of the families Noctuidae, Tortricidae, Plutellidae, and Chrysomelidae. Appl. Environ. Microbiol. 72 (2006) 4796-4804
50. Sambrook J., and Russell D.W. Molecular Cloning: A laboratory Manual. third ed. (2001), Cold Spring Harbor Laboratory Press, New York
51. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., and Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62 (1998) 775-806
52. Shevelev A.B., Svarinsky M.A., Karasin A.I., Kogan Ya N., Chestukhina G.G., and Stepanov V.M. Primary structure of cryX, the novel delta-endotoxin-related gene from Bacillus thuringiensis spp. galleriae. FEBS Lett. 336 (1993) 79-82
53. Shin B.S., Park S.H., Choi S.K., Koo B.T., Lee S.T., and Kim J.I. Distribution of cryV-type insecticidal protein genes in Bacillus thuringiensis and cloning of cryV-type genes from Bacillus thuringiensis subsp. kurstaki and Bacillus thuringiensis subsp. entomocidus. Appl. Environ. Microbiol. 61 (1995) 2402-2407
54. Song F., Zhang J., Gu A., Wu Y., Han L., He K., Chen Z., Yao J., Hu Y., Li G., and Huang D. Identification of cry1I-type genes from Bacillus thuringiensis strains and characterization of a novel cry1I-type gene. Appl. Environ. Microbiol. 69 (2003) 5207-5211
55. Stewart G.S.A.B., Johnstone K., Hagelberg E., and Ellar D.J. Commitment of bacterial spores to germinate. A measure of the trigger reaction. Biochem. J. 196 (1981) 101-106
56. Tailor R., Tippett J., Gibb G., Pells S., Pike D., Jordan L., and Ely S. Identification and characterization of a novel Bacillus thuringiensis δ-endotoxin entomocidal to coleopteran and lepidopteran larvae. Mol. Microbiol. 6 (1992) 1211-1217
57. Thomas W.E., and Ellar D.J. Bacillus thuringiensis var israelensis crystal δ-endotoxin: effects on insect and mammalian cells in vitro and in vivo. J. Cell Sci. 60 (1983) 181-197
58. Thompson J.D., Higgins D.G., and Gibson T.J. Clustal W-Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
59. Tounsi S., and Jaoua S. Identification of a promoter for the crystal protein-encoding gene cry1Ia from Bacillus thuringiensis subsp. kurstaki. FEMS Microbiol. Lett. 208 (2002) 215-218
60. Tounsi S., Zouari N., and Jaoua S. Cloning and study of the expression of a novel cry1Ia -type gene from Bacillus thuringiensis subsp. kurstaki. J. Appl. Microbiol. 95 (2003) 23-28
61. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from acrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76 (1979) 4350-4354
62. Van Rie J., Jansens S., Höfte H., Degheele D., and Van Mellaert H. Specificity of Bacillus thuringiensis delta-endotoxins. Importance of specific receptors on the brush border membrane of the midgut of target insects. Eur. J. Biochem. 186 (1989) 239-247
63. Vilchez S., Jacoby J., and Ellar D.J. Display of biologically functional insecticidal toxin on the surface of lambda phage. Appl. Environ. Microbiol. 70 (2004) 6587-6594
64. Wang J., Boets A., Van Rie J., and Ren G. Characterization of cry1, cry2, and cry9 genes in Bacillus thuringiensis isolates from China. J. Invertebr. Pathol. 82 (2003) 63-71
65. Ward E.S., and Ellar D.J. Assignment of the δ-endotoxin of Bacillus thuringiensis var israelensis to a specific plasmid by curing analysis. FEBS Lett. 158 (1983) 45-49
66. Wasano N., Kim K.-H., and Ohba M. Delta-endotoxin proteins associated with spherical parasporal inclusions of the four Lepidoptera-specific Bacillus thuringiensis strains. J. Appl. Microbiol. 84 (1998) 501-508
67. Wasano N., and Ohba M. Assignment of delta-endotoxin genes of the four lepidoptera-specific Bacillus thuringiensis strains that produce spherical parasporal inclusions. Curr. Microbiol. 37 (1998) 408-411
68. Wasano N., Ohba M., and Miyamoto K. Two delta-endotoxin genes, cry9Da and a novel related gene, commonly occurring in Lepidoptera-specific Bacillus thuringiensis Japanese isolates that produce spherical parasporal inclusions. Curr. Microbiol. 42 (2001) 129-133
69. Wasano N., Saitoh H., Maeda M., Ohgushi A., Mizuki E., and Ohba M. Cloning and characterization of a novel gene cry9Ec1 encoding lepidopteran-specific parasporal inclusion protein from a Bacillus thuringiensis serovar galleriae strain. Can. J. Microbiol. 51 (2005) 988-995
70. Wasano N., Yasunaga-Aoki C., Sato R., Ohba M., Kawarabata T., and Iwahana H. Spherical parasporal inclusions of the Lepidoptera-specific and Coleoptera-specific Bacillus thuringiensis strains: a comparative electron microscopic study. Curr. Microbiol. 40 (2000) 128-131
71. Wei J.Z., Hale K., Carta L., Platzer E., Wong C., Fang S.C., and Aroian R.V. Bacillus thuringiensis crystal proteins that target nematodes. Proc. Natl. Acad. Sci. USA 100 (2003) 2760-2765
72. Wolfersberger M., Luethy P., Maurer A., Parenti P., Sacchi F.V., Giordana B., and Hanozet G.M. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comp. Biochem. Physiol. 86A (1987) 301-308
73. Yousten A.A. Bacillus sphaericus: microbiological factors related to its potential as a mosquito larvicide. Adv. Biotechnol. Proc. 3 (1984) 315-343
74. Zhong C., Ellar D.J., Bishop A., Johnson C., Lin S., and Hart E.R. Characterization of a Bacillus thuringiensis delta-endotoxin which is toxic to insects in three orders. J. Invertebr. Pathol. 76 (2000) 131-139