Are nematodes a missing link in the confounded ecology of the entomopathogen Bacillus thuringiensis?

Trends in Microbiology

Volumn 23, Issue 6, 2015, Pages 341-346

  Ruan, Lifang ^a   Crickmore, Neil ^b   Peng, Donghai ^a   Sun, Ming ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Bacillus thuringiensis; Ecology; Host; Nematodes

Indexed keywords

BACTERIAL PROTEIN; CRY PROTEIN; INSECTICIDE; UNCLASSIFIED DRUG;

BACILLUS ANTHRACIS; BACILLUS CEREUS; BACILLUS THURINGIENSIS; BACTERIAL COLONIZATION; BACTERIAL ENDOSPORE; BACTERIAL REPRODUCTION; BACTERIAL SURVIVAL; COEVOLUTION; ECOLOGICAL NICHE; ENTOMOPATHOGENIC BACTERIUM; EVOLUTIONARY ADAPTATION; HOST PATHOGEN INTERACTION; HOST RANGE; INSECTICIDAL ACTIVITY; NEMATODE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOIL MICROFLORA; SPECIES DISTRIBUTION; ANIMAL; CLASSIFICATION; ECOSYSTEM; ENDOPHYTE; INSECT; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); HEXAPODA; NEMATODA;

ANIMALS; BACILLUS THURINGIENSIS; ECOSYSTEM; ENDOPHYTES; HOST-PATHOGEN INTERACTIONS; INSECTS; NEMATODA; SOIL MICROBIOLOGY;

EID: 84930928274     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.02.011     Document Type: Review

References (87)

1. Raymond B., et al. Bacillus thuringiensis: an impotent pathogen?. Trends Microbiol. 2010, 18:189-194.
2. ArgÔlo-Filho R., Loguercio L. Bacillus thuringiensis is an environmental pathogen and host-specificity has developed as an adaptation to human-generated ecological niches. Insects 2013, 5:62-91.
3. Pardo-Lopez L., et al. Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol. Rev. 2013, 37:3-22.
4. Bravo A., et al. Evolution of Bacillus thuringiensis Cry toxins insecticidal activity. Microb. Biotechnol. 2013, 6:17-26.
5. Crickmore N., et al. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998, 62:807-813.
6. Azzouz H., et al. Selection and characterisation of an HD1-like Bacillus thuringiensis isolate with a high insecticidal activity against Spodoptera littoralis (Lepidoptera: Noctuidae). Pest Manag. Sci. 2014, 70:1192-1201.
7. Gorashi N.E., et al. Identification and characterization of the Sudanese Bacillus thuringiensis and related bacterial strains for their efficacy against Helicoverpa armigera and Tribolium castaneum. Indian J. Exp. Biol. 2014, 52:637-649.
8. van Frankenhuyzen K. Insecticidal activity of Bacillus thuringiensis crystal proteins. J. Invertebr. Pathol. 2009, 101:1-16.
9. van Frankenhuyzen K. Cross-order and cross-phylum activity of Bacillus thuringiensis pesticidal proteins. J. Invertebr. Pathol. 2013, 114:76-85.
10. Kuroda S., et al. Parasporin 1Ac2, a novel cytotoxic crystal protein isolated from Bacillus thuringiensis B0462 Strain. Curr. Microbiol. 2013, 66:475-480.
11. Zheng J.S., et al. Differentiation of Bacillus anthracis, B. cereus, and B. thuringiensis on the basis of the csaB gene reflects host source. Appl. Environ. Microb. 2013, 79:3860-3863.
12. Juarez-Perez V.M., et al. PCR-based approach for detection of novel Bacillus thuringiensis cry genes. Appl. Environ. Microbiol. 1997, 63:2997-3002.
13. Noguera P.A., Ibarra J.E. Detection of new cry genes of Bacillus thuringiensis by use of a novel PCR primer system. Appl. Environ. Microbiol. 2010, 76:6150-6155.
14. Ye W.X., et al. Mining new crystal protein genes from Bacillus thuringiensis on the basis of mixed plasmid-enriched genome sequencing and a computational pipeline. Appl. Environ. Microbiol. 2012, 78:4795-4801.
15. Adang M.J., et al. Diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Adv. Insect Physiol. 2014, 47:39-87.
16. Raymond B., et al. Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathog. 2010, 6:e1000905.
17. Lu Y.H., et al. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 2010, 328:1151-1154.
18. Shojaaddini M., et al. A Bacillus thuringiensis strain producing epizootics on Plodia interpunctella: a case study. J. Stored Prod. Res. 2012, 48:52-60.
19. Baig D.N., Mehnaz S. Determination and distribution of cry-type genes in halophilc Bacillus thuringiensis isolates of Arabian Sea sedimentary rocks. Microbiol. Res. 2010, 165:376-383.
20. Prabhakar A., Bishop A.H. Invertebrate pathogenicity and toxin-producing potential of strains of Bacillus thuringiensis endemic to Antarctica. J. Invertebr. Pathol. 2011, 107:132-138.
21. Fang Y.J., et al. A pangenomic study of Bacillus thuringiensis. J. Genet. Genomics 2011, 38:567-576.
22. Guinebretiere M.H., et al. Ecological diversification in the Bacillus cereus group. Environ. Microbiol. 2008, 10:851-865.
23. Raymond B., et al. The dynamics of cooperative bacterial virulence in the field. Science 2012, 337:85-88.
24. Deng C., et al. Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain. ISME J. 2015, 9:286-296.
25. Vidal-Quist J.C., et al. Bacillus thuringiensis colonises plant roots in a phylogeny-dependent manner. FEMS Microbiol. Ecol. 2013, 86:474-489.
26. Bizzarri M.F., Bishop A.H. The ecology of Bacillus thuringiensis on the phylloplane: colonization from soil, plasmid transfer, and interaction with larvae of Pieris brassicae. Microb. Ecol. 2008, 56:133-139.
27. Prabhakar A., Bishop A.H. Effect of Bacillus thuringiensis naturally colonising Brassica campestris var. chinensis leaves on neonate larvae of Pieris brassicae. J. Invertebr. Pathol. 2009, 100:193-194.
28. Maduell P., et al. B. thuringiensis is a poor colonist of leaf surfaces. Microb. Ecol. 2008, 55:212-219.
29. Botelho Praca L., et al. Endophytic colonization by Brazilian strains of Bacillus thuringiensis on cabbage seedlings grown in vitro. Bt. Res. 2012, 3:11-19.
30. Rasko D.A., et al. Genomics of the Bacillus cereus group of organisms. FEMS Microbiol. Rev. 2005, 29:303-329.
31. Martin P.A., Travers R.S. Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl. Environ. Microbiol. 1989, 55:2437-2442.
32. Hendriksen N.B., Carstensen J. Long-term survival of Bacillus thuringiensis subsp. kurstaki in a field trial. Can. J. Microbiol. 2013, 59:34-38.
33. Vilas-Boas L.A., et al. Survival and conjugation of Bacillus thuringiensis in a soil microcosm. FEMS Microbiol. Ecol. 2000, 31:255-259.
34. Maslen N.R., Convey P. Nematode diversity and distribution in the southern maritime Antarctic: clues to history?. Soil Biol. Biochem. 2006, 38:3141-3151.
35. Jouzani G.S., et al. Molecular detection of nematicidal crystalliferous Bacillus thuringiensis strains of Iran and evaluation of their toxicity on free-living and plant-parasitic nematodes. Can. J. Microbiol. 2008, 54:812-822.
36. Hu Y., et al. Discovery of a highly synergistic anthelmintic combination that shows mutual hypersusceptibility. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:5955-5960.
37. Luo H., et al. The effects of Bacillus thuringiensis Cry6A on the survival, growth, reproduction, locomotion, and behavioral response of Caenorhabditis elegans. Appl. Microbiol. Biotechnol. 2013, 97:10135-10142.
38. Wang P.X., et al. Complete genome sequence of Bacillus thuringiensis YBT-1518, a typical strain with high toxicity to nematodes. J. Biotechnol. 2014, 171:1-2.
39. Guo S.X., et al. New strategy for isolating novel nematicidal crystal protein genes from Bacillus thuringiensis strain YBT-1518. Appl. Environ. Microbiol. 2008, 74:6997-7001.
40. Iatsenko I., et al. Identification of distinct Bacillus thuringiensis 4A4 nematicidal factors using the model nematodes Pristionchus pacificus and Caenorhabditis elegans. Toxins 2014, 6:2050-2063.
41. Iatsenko I., et al. Bacillus thuringiensis DB27 produces two novel protoxins, Cry21Fa1 and Cry21Ha1, which act synergistically against nematodes. Appl. Environ. Microbiol. 2014, 80:3266-3275.
42. Liu Y.Y., et al. High-quality draft genome sequence of nematocidal Bacillus thuringiensis Sbt003. Stand. Genomic Sci. 2014, 9:624-631.
43. Lenane I.J., et al. A pair of adjacent genes, cry5Ad and orf2-5Ad, encode the typical N- and C-terminal regions of a Cry5Adelta-endotoxin as two separate proteins in Bacillus thuringiensis strain L366. FEMS Microbiol. Lett. 2008, 278:115-120.
44. Liu X., et al. Draft genome sequence of Bacillus thuringiensis NBIN-866 with high nematocidal activity. Genome Announc. 2014, 2:e00429-e00514.
45. Zhang L.L., et al. Biological activity of Bacillus thuringiensis (Bacillales: Bacillaceae) chitinase against Caenorhabditis elegans (Rhabditida: Rhabditidae). J. Econ. Entomol. 2014, 107:551-558.
46. Luo X.X., et al. Bacillus thuringiensis metalloproteinase Bmp1 functions as a nematicidal virulence factor. Appl. Environ. Microbiol. 2013, 79:460-468.
47. Devidas P., Rehberger L.A. The effects of exotoxin (thuringiensin) from Bacillus thuringiensis on Meloidogyne incognita and Caenorhabditis elegans. Plant and Soil 1992, 145:115-120.
48. Garsin D.A., et al. A simple model host for identifying Gram-positive virulence factors. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10892-10897.
49. Zhou M., et al. Lactobacillus zeae protects Caenorhabditis elegans from enterotoxigenic Escherichia coli-caused death by inhibiting enterotoxin gene expression of the pathogen. PLoS ONE 2014, 9:e89004.
50. Cinar H.N., et al. Vibrio cholerae hemolysin is required for lethality, developmental delay, and intestinal vacuolation in Caenorhabditis elegans. PLoS ONE 2010, 5:e11558.
51. Yang J.K., et al. Nematicidal enzymes from microorganisms and their applications. Appl. Microbiol. Biotechnol. 2013, 97:7081-7095.
52. Murphy K., et al. Genome mining for radical SAM protein determinants reveals multiple sactibiotic-like gene clusters. PLoS ONE 2011, 6:e20852.
53. Begley M., et al. Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl. Environ. Microbiol. 2009, 75:5451-5460.
54. Gohar M., et al. A comparative study of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis extracellular proteomes. Proteomics 2005, 5:3696-3711.
55. Schulte R.D., et al. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7359-7364.
56. Borgonie G., et al. Germination of Bacillus thuringiensis spores in bacteriophagous nematodes (Nematoda: Rhabditida). J. Invertebr. Pathol. 1995, 65:61-67.
57. Kho M.F., et al. The pore-forming protein Cry5B elicits the pathogenicity of Bacillus sp. against Caenorhabditis elegans. PLoS ONE 2011, 6:e29122.
58. Zhang F.J., et al. In vitro uptake of 140 kDa Bacillus thuringiensis nematicidal crystal proteins by the second stage juvenile of Meloidogyne hapla. PLoS ONE 2012, 7:e38534.
59. Sinott M.C., et al. Bacillus spp. toxicity against Haemonchus contortus larvae in sheep fecal cultures. Exp. Parasitol. 2012, 132:103-108.
60. Kotze A.C., et al. Toxicity of Bacillus thuringiensis to parasitic and free-living life-stages of nematode parasites of livestock. Int. J. Parasitol. 2005, 35:1013-1022.
61. Urban J.F., et al. Bacillus thuringiensis-derived Cry5B has potent anthelmintic activity against ascaris suum. PLoS Negl. Trop. Dis. 2013, 7:e2263.
62. Wei J.Z., et al. Bacillus thuringiensis crystal proteins that target nematodes. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2760-2765.
63. Schulte R.D., et al. Increased responsiveness in feeding behaviour of Caenorhabditis elegans after experimental coevolution with its microparasite Bacillus thuringiensis. Biol. Lett. 2012, 8:234-236.
64. Schulte R.D., et al. Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis. Proc. Biol. Sci. 2011, 278:2832-2839.
65. Schulte R.D., et al. Host-parasite coevolution favours parasite genetic diversity and horizontal gene transfer. J. Evol. Biol. 2013, 26:1836-1840.
66. Masri L., et al. Sex differences in host defence interfere with parasite-mediated selection for outcrossing during host-parasite coevolution. Ecol. Lett. 2013, 16:461-468.
67. Suzuki M.T., et al. Fate of Bacillus thuringiensis strains in different insect larvae. Can. J. Microbiol. 2004, 50:973-975.
68. Dubois T., et al. Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog. 2012, 8:e1002629.
69. McMahon L., et al. Two sets of interacting collagens form functionally distinct substructures within a Caenorhabditis elegans extracellular matrix. Mol. Biol. Cell 2003, 14:1366-1378.
70. Gegeckas A., et al. Keratinolytic proteinase from Bacillus thuringiensis AD-12. Int. J. Biol. Macromol. 2014, 69:46-51.
71. Chung M.C., et al. Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J. Biol. Chem. 2006, 281:31408-31418.
72. Gohar M., et al. Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2002, 2:784-791.
73. Murfin K.E., et al. Nematode-bacterium symbioses-cooperation and conflict revealed in the "Omics" age. Biol. Bull. 2012, 223:85-102.
74. Nielsen-LeRoux C., et al. How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts. Curr. Opin. Microbiol. 2012, 15:220-231.
75. Blackburn M.B., et al. The occurrence of photorhabdus-like toxin complexes in Bacillus thuringiensis. PLoS ONE 2011, 6:e18122.
76. Nishanth Kumar S., et al. Purification of an antifungal compound, cyclo(l-Pro-d-Leu) for cereals produced by Bacillus cereus subsp. thuringiensis associated with entomopathogenic nematode. Microbiol. Res. 2013, 168:278-288.
77. Nishanth Kumar S., et al. Cyclic dipeptides from rhabditid entomopathogenic nematode-associated Bacillus cereus have antimicrobial activities. World J. Microbiol. Biotechnol. 2014, 30:439-449.
78. Kumar S.N., et al. Purification and identification of two antifungal cyclic dipeptides from Bacillus cereus subsp thuringiensis associated with a rhabditid entomopathogenic nematode especially against Fusarium oxysporum. J. Enzyme Inhib. Med. Chem. 2014, 29:190-197.
79. Rae R., et al. Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences. J. Exp. Biol. 2008, 211:1927-1936.
80. Laaberki M.H., Dworkin J. Death and survival of spore-forming bacteria in the Caenorhabditis elegans intestine. Symbiosis 2008, 46:95-100.
81. Gomez P., Buckling A. Bacteria-phage antagonistic coevolution in soil. Science 2011, 332:106-109.
82. Medini D., et al. The microbial pan-genome. Curr. Opin. Genet. Dev. 2005, 15:589-594.
83. Schunemann R., et al. Mode of action and specificity of Bacillus thuringiensis toxins in the control of caterpillars and stink bugs in soybean Culture. ISRN Microbiol. 2014, 2014:135675.
84. Kao C.Y., et al. Global functional analyses of cellular responses to pore-forming toxins. PLoS Pathog. 2011, 7:e1001314.
85. Rasmann S., et al. Ecology and evolution of soil nematode chemotaxis. J. Chem. Ecol. 2012, 38:615-628.
86. Marahatta S.P., et al. Effects of the integration of sunn hemp and soil solarization on plant-parasitic and free-living nematodes. J. Nematol. 2012, 44:72-79.
87. Neher D.A. Ecology of plant and free-living nematodes in natural and agricultural soil. Annu. Rev. Phytopathol. 2010, 48:371-394.