Abstract
Bacillus thuringiensis (Bt) is a Gram-positive, spore-forming, soil bacterium, which is very popular bio-control agent in agricultural and forestry. In general, B. thuringiensis secretes an array of insecticidal proteins including toxins produced during vegetative growth phase (such as secreted insecticidal protein, Sip; vegetative insecticidal proteins, Vip), parasporal crystalline δ-endotoxins produced during vegetative stationary phase (such as cytolytic toxin, Cyt; and crystal toxin, Cry), and β-exotoxins. Till date, a wide spectrum of Cry proteins has been reported and most of them belong to three-domain-Cry toxins, Bin-like toxin, and Etx_Mtx2-like toxins. To the best of our knowledge, neither Bt insecticidal toxins are exclusive to Bt nor all the strains of Bt are capable of producing insecticidal Bt toxins. The lacuna in their latest classification has also been discussed. In this review, the updated information regarding the insecticidal Bt toxins and their different mode of actions were summarized. Before applying the Bt toxins on agricultural field, the non-specific effects of toxins should be investigated. We also have summarized the problem of insect resistance and the strategies to combat with this problem. We strongly believe that this information will help a lot to the budding researchers in the field of modern pest control biotechnology.
Similar content being viewed by others
References
Ajamhassani M, Ghadamyary M, Borovsky D (2011) Effect of trypsin modulating oostatic factor (TMOF) on trypsin and chymotrypsin in Glyphodes pyloalis Walker (Lep.: Pyralidae) and Hyphantria cunea Drury (Lep.: Arctiidae). Pestycydy/Pesticides 1–4:35–39
Altieri MA, Rosset P (1999) Strengthening the case for why biotechnology will not help the developing world: a response to McGloughlin. AgBioForum 2:226–236
Azizoglu U, Yılmaz S, Ayvaz A, Karabörklü S (2015) Effects of Bacillus thuringiensis subsp. kurstaki HD1 spore-crystal mixture on the adults of egg parasitoid Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Biotechnol Biotechnol Equip 29:653–658
Baranek J, Kaznowski A, Konecka E, Naimov S (2015) Activity of vegetative insecticidal proteins Vip3Aa58 and Vip3Aa59 of Bacillus thuringiensis against lepidopteran pests. J Invertebr Pathol 130:72–81
Ben-Dov E (2014) Bacillus thuringiensis subsp. israelensis and its dipteran-specific toxins. Toxins 6:1222–1243
Berlitz DL, de Athayde Sau D, Machado V, de Cássia Santin R, Guimarães AM, Matsumura ATS, Ribeiro BM, Fiuza LM (2013) Bacillus thuringiensis: molecular characterization, ultrastructural and nematoxicity to Meloidogyne sp. J Biopest 6:120–128
Berry C (2012) Lysinibacillus sphaericus, as an insect pathogen. J Invertebr Pathol 109:1–10
Bøhn T, Primicerio R, Hessen DO, Traavik T (2008) Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch Environ Contam Toxicol 55:584–592
Brandt SL, Coudron TA, Habibi J, Brown GR, Ilagan OM, Wagner RM, Wright MK, Backus EA, Huesing JE (2004) Interaction of two Bacillus thuringiensis delta-endotoxins with the digestive system of lygus hesperus. Curr Microbiol 48(1):1–9
Brasseur K, Auger P, Asselin E, Parent S, Côté J-C, Sirois M (2015) Parasporin-2 from a new Bacillus thuringiensis 4R2 strain induces caspases activation and apoptosis in human cancer cells. PLoS One 10(8):e0135106. https://doi.org/10.1371/journal.pone.0135106
Braun R, Bennett DJ, Secretariat EFB, Delft O (2001) Antibiotic resistance markers in genetically modified (GM) crops. Task group on public perceptions of biotechnology, European Federation of Biotechnology
Bravo A, Soberón M (2008) How to cope with resistance to Bt toxins? Trends Biotechnol 26:573–579
Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435
Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431
Bravo A, Gómez I, Porta H, García-Gómez BI, Rodriguez-Almazan C, Pardo L, Soberón M (2013) Evolution of Bacillus thuringiensis Cry toxins insecticidal activity. Microbial Biotechnol 6(1):17–26
Cadavid-Restrepo G, Sahaza J, Orduz S (2012) Treatment of an Aedes aegypti colony with the Cry11Aa toxin for 54 generations results in the development of resistance. The Memórias do Inst Oswaldo Cruz 107(1):74–79
Cantón PE, López-Díaz JA, Gill SS, Bravo A, Soberón M (2014) Membrane binding and oligomer membrane insertion are necessary but insufficient for Bacillus thuringiensis Cyt1Aa toxicity. Peptides 53:286–291
Carlton BC, Gawron-Burke C (1993) Genetic improvement of Bacillus thuringiensis for bioinsecticide development. In: Kim L (ed) Advanced Engineered Biopesticides. Marcel Dekker Inc, NY, pp 43–61
Castagnola A, Patricia Stock S (2014) Common virulence factors and tissue targets of entomopathogenic bacteria for biological control of lepidopteran pests. Insects 5(1):139–166
Cerstiaens A, Verleyen P, van Rie J, van Kerkhove E, Schwartz J-L, Laprade R, de Loof A, Schoofs L (2001) Effect of Bacillus thuringiensis Cry1 toxins in insect hemolymph and their neurotoxicity in brain cells of Lymantria dispar. Appl Environ Microbiol 67:3923–3927
Chakroun M, Banyuls N, Walsh T, Downes S, James B, Ferré J (2016) Characterization of the resistance to Vip3Aa in Helicoverpa armigera from Australia and the role of midgut processing and receptor binding. Sci Rep 6:24311
Chougule NP, Li H, Liu S, Linz LB, Narva KE, Meade T, Bonning BC (2013) Retargeting of the Bacillus thuringiensis toxin Cyt2Aa against hemipteran insect pests. Proc Natl Acad Sci USA 110:218465–218470
Chougule NP, Bonning BC (2012) Toxins for transgenic resistance to hemipteran pests. Toxins (Basel) 4(6):405–429
Coates BS, Sumerford DV, Siegfried BD, Hellmich RL, Abel CA (2013) Unlinked genetic loci control the reduced transcription of aminopeptidase N 1 and 3 in the European corn borer and determine tolerance to Bacillus thuringiensis Cry1Ab toxin. Insect Biochem Mol Biol 43(12):1152–1160
Contreras E, Rausell C, Real MD (2013) Proteome response of Tribolium castaneum larvae to Bacillus thuringiensis toxin producing strains. PLoS One 8(1):e55330. https://doi.org/10.1371/journal.pone.0055330
Crickmore N, Zeigler DR, Feitelson J, Schnepf E, Van-rie J, Lereclus D, Baum J, Dean DH (1998) Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol Mol Biol Rev 62:807–813
Crickmore N, Zeigler DR, Schnepf E, van Rie J, Lereclus D, Baum J, Bravo A, Dean DH (2014) Bacillus thuringiensis toxin nomenclature. Available online: http://www.lifesci.sussex.ac.uk/Home/Neil_Crickmore/Bt/
de Maagd RA, Bosch D, Stiekema W (1999) Bacillus thuringiensis toxin-mediated insect resistance in plants. Trends Plant Sci 4:9–13
de Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Ann Rev Genet 37:409–433
de Schrijver A, De Clercq P, de Maagd RA, van Frankenhuyzen K (2015) Relevance of Bt toxin interaction studies for environmental risk assessment of genetically modified crops. Plant Biotechnol J 13:1221–1223
Deist BR, Rausch MA, Fernandez-Luna MT, Adang MJ, Bonning BC (2014) Bt toxin modification for enhanced efficacy. Toxins 6(10):3005–3027
Doggett NA, Stubben CJ, Chertkov O, Bruce DC, Detter JC, Johnson SL, Han CS (2013) Complete genome sequence of Bacillus thuringiensis serovar israelensis strain HD-789. Genome Announce 1:e01023-13
Ekobu M, Solera M, Kyamanywa S, Mwanga RO, Odongo B, Ghislain M, Moar WJ (2010) Toxicity of seven Bacillus thuringiensis Cry proteins against Cylas puncticollis and Cylas brunneus (Coleoptera: Brentidae) using a novel artificial diet. J Econ Entomol 103:1493–1502
Elleuch J, Jaoua S, Darriet F, Chandre F, Tounsi S, Zghal RZ (2015) Cry4Ba and Cyt1Aa proteins from Bacillus thuringiensis israelensis: Interactions and toxicity mechanism against Aedes aegypti. Toxicon 104:83–90
Elzak MEA (2016) Resistance to Bt crops; influence, mechanisms and management strategies. Biotechnol Mol Biol Rev 11:1–5
Endo H, Tanaka S, Imamura K, Adegawa S, Kikuta S, Sato R (2017) Cry toxin specificities of insect ABCC transporters closely related to lepidopteran ABCC2 transporters. Peptides 98:86–92
Ferry N, Edwards MG, Mulligan EA, Emami K, Petrova AS, Frantescu M, Davison GM, Gatehouse AMR (2004) Engineering resistance to insect pests. In: Christou P, Klee H (eds) Handbook of Plant Biotechnology. Wiley, Chichester, pp 373–394
Franklin MT, Nieman CL, Janmaat AF, Soberón M, Bravo A, Tabashnik BE, Myers JH (2009) Modified Bacillus thuringiensis toxins and a hybrid B. thuringiensis strain counter greenhouse-selected resistance in Trichoplusia ni. Appl Environ Microbiol 75:5739–5741
Guo CH, Zhao ST, Ma Y, Hu JJ, Han XJ, Chen J, Lu MZ (2012) Bacillus thuringiensis Cry3Aa fused to a cellulase-binding peptide shows increased toxicity against the longhorned beetle. Appl Environ Microbiol 93:1249–1256
Han G, Li X, Zhang T, Zhu X, Li J (2015) Cloning and tissue-specific expression of a chitin deacetylase gene from Helicoverpa armigera (Lepidoptera: Noctuidae) and its response to Bacillus thuringiensis. J Insect Sci 15(1):95
Hayakawa T, Yoneda N, Okada K, Higaki A, Howlader MTH, Ide T (2016) Bacillus thuringiensis Cry11Ba works synergistically with Cry4Aa but not with Cry11Aa for toxicity against mosquito Culex pipiens (Diptera: Culicidae) larvae. Appl Entomol Zool. https://doi.org/10.1007/s13355-016-0454-z
Höfte H, Whiteley HR (1989) Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev 53(2):242–255
Hussein HM, Habuštová O, Turanli F, Sehnal F (2006) Potato expressing beetle–specific Bacillus thuringienis Cry3Aa toxin reduces performance of a moth. J Chem Ecol 32:1–13
Ibrahim MA, Griko N, Junker M, Bulla LA (2010) Bacillus thuringiensis: a genomics and proteomics perspective. Bioeng Bugs 1(1):31–50
Kelker MS, Berry C, Evans SL, Pai R, McCaskill DG, Wang NX, Russell JC, Baker MD, Yang C, Pflugrath JW, Wade M, Wess TJ, Narva KE (2014) Structural and biophysical characterization of Bacillus thuringiensis insecticidal proteins Cry34Ab1 and Cry35Ab1. PLoS One 9(11):e112555
Land M, Miljand M (2014) Biological control of mosquitoes using Bacillus thuringiensis israelensis: a pilot study of effects on target organisms, non-target organisms and humans. Mistra EviEM Pilot Study PS4 (www.eviem.se)
Lawo NC, Wäckers FL, Romeis J (2009) Indian Bt cotton varieties do not affect the performance of cotton aphids. PLoS One 4:e4804
Lee SB (2013) Toxin binding receptors and the mode of action of Bacillus thuringiensis subsp. israelensis Cry toxins. UC Riverside: Environmental Toxicology. Retrieved from: http://escholarship.org/uc/item/6cr35910
Levinson BL, Kasyan KJ, Chiu SS, Currier TC, González JM Jr (1990) Exotoxin, β-exotoxin production, plasmids encoding & β Identification of and a new exotoxin in Bacillus thuringiensis by using high performance liquid chromatography. J Bacteriol 172:3172–3179
Liu X, Ruan L, Peng D, Li L, Sun M, Yu Z (2014) Thuringiensin: a thermostable secondary metabolite from Bacillus thuringiensis with insecticidal activity against a wide range of insects. Toxins 6:2229–2238
Losey JE, Raynor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399:214
Maghari BM, Ardekani AM (2011) Genetically modified foods and social concerns. Avicenna J Med Biotechnol 3:109
Obeidat M, Khyami-Horani H, Al-Moman F (2012) δ-Exotoxins and & βToxicity of Bacillus thuringiensis endotoxins to Drosophila melanogaster, Ephestia kuhniella and human erythrocytes. Afr J Biotechnol 11(46):10504–10512
Pacheco S, Gomez I, Arenas I, Saab-Rincon G, Rodriguez-Almazan C, Gill SS, Bravo A, Soberon M (2009) Domain II loop 3 of Bacillus thuringiensis Cry1Ab toxin is involved in a “ping-pong” binding mechanism with Manduca sexta aminopetidase-N and cadherin receptors. J Biol Chem 284:32750–32757
Palma L (2015) Protocol for the fast isolation and identification of insecticidal Bacillus thuringiensis strains from soil. Bt Res 6:1–3
Palma L, Muñoz D, Berry C, Murillo J, Caballero P (2014) Draft genome sequences of two Bacillus thuringiensis strains and characterization of a putative 41.9-kDa insecticidal toxin. Toxins 6:1490–1504
Pardo-López L, Soberón M, Bravo A (2013) Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37:3–22
Park Y, González-Martínez RM, Navarro-Cerrillo G, Chakroun M, Kim Y, Ziarsolo P, Blanca J, Cañizares J, Ferré J, Herrero S (2014) ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biol 14:46
Reed GL, Jensen AS, Riebe J, Head G, Duan JJ (2001) Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts. Entomol Exp Appl 100:89–100
Resende DC, Mendes SM, Rosangela C, Marucci RC, de Carvalho Silva A, Campanha MM, Waquil JM (2016) Does Bt maize cultivation affect the non-target insect community in the agro ecosystem? Rev Bras Entomol 60:82–93
Rodrigo-Simon A, de Maagd RA, Avilla C, Bakker PL, Molthoff J, González-Zamora JE, Ferre J (2006) Lack of detrimental effects of Bacillus thuringiensis Cry toxins on the insect predator Chrysoperla carnea: a toxicological, histopathological, and biochemical analysis. Appl Environ Microbiol 72:1595–1603
Romeis J, Meissle M, Naranjo SE, Li Y, Bigler F (2014) The end of a myth—Bt (Cry1Ab) maize does not harm green lacewings. Front Plant Sci 5:391
Sato K, Yoshiga T, Hasegawa K (2014) Activated and inactivated immune responses in Caenorhabditis elegans against Photorhabdus luminescens TT01. Springer Plus 3:274
Sattar S, Maiti MK (2011) Molecular characterization of a novel vegetative insecticidal protein from Bacillus thuringiensis effective against sap-sucking insect pest. J Microbiol Biotechnol 21:937–946
Schnepf HE, Whiteley HR (1981) Cloning and expression of the Bacillus thuringiensis crystal protein gene in Escherichia coli. Proc Natl Acad Sci USA 78:2893–2897
Sena JAD, Hernandez-Rodrigues CS, Ferre J (2009) Interaction of Bacillus thuringiensis Cry1 and Vip3A proteins with Spodoptera frugiperda midgut binding sites. Appl Environ Microbiol 75(7):2236–2237
Silvia Denise PB, Eduardo PM, Benjamín VC (2013) Recombinant protein detection and its content in total protein, lipids and toxic antinutritional substances in Mexican maize. Health 5:9–13
Soberón M, Pardo L, Muñóz-Garay C, Sánchez J, Gómez I, Porta H, Bravo A (2010) Pore formation by Cry toxins. Adv Exp Med Biol 677:127–142
Srisucharitpanit K, Yao M, Promdonkoy B, Chimnaronk S, Tanaka I, Boonserm P (2014) Crystal structure of BinB: a receptor binding component of the binary toxin from Lysinibacillus sphaericus. Proteins 82:2703–2712
Szczesny P, Iacovache I, Muszewska A, Ginalski K, van der Goot FG, Grynberg M (2011) Extending the aerolysin family: from bacteria to vertebrates. PLoS One 6(6):e20349. https://doi.org/10.1371/journal.pone.0020349
Tabashnik BE, Sisterson MS, Ellsworth PC, Dennehy TJ, Antilla L, Liesner L, Whitlow M, Staten RT, Fabrick JA, Unnithan GC, Yelich AJ, Ellers-Kirk C, Harpold VS, Li X, Carrière Y (2010) Suppressing resistance to Bt cotton with sterile insect releases. Nat Biotechnol 28(12):1304–1307
Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521
Tabashnik BE, Zhang M, Fabrick JA, Wu Y, Gao M, Huang F, Wei J, Zhang J, Yelich A, Unnithan GC, Bravo A, Soberón M, Carrière Y, Li X (2015) Dual mode of action of Bt proteins: protoxin efficacy against resistant insects. Sci Rep 5:15107. https://doi.org/10.1038/srep15107
Xu C, Wang B-C, Yu Z, Sun M (2014) Structural Insights into Bacillus thuringiensis Cry. Cyt and Parasporin Toxins. Toxins 6(9):2732–2770
Yudina TG, Brioukhanov AL, Zalunin IA, Revina LP, Shestakov AI, Voyushina NE, Chestukhina GG, Netrusov AI (2007) Antimicrobial activity of different proteins and their fragments from Bacillus thuringiensis parasporal crystals against clostridia and archaea. Anaerobe 13:6–13
Zhang Y, Zhang J, Lan J, Wang J, Liu J, Yang M (2016) Temporal and spatial changes in Bt toxin expression in Bt-transgenic poplar and insect resistance in field tests. J For Res 27:1249–1256
Acknowledgements
Authors are very much thankful to Visva Bharati University, India, University of Calcutta, India, and Gauhaati University, India for proving necessary supports. This work is not funded by any agencies. Authors express their sincere respects to the honorable reviewers for their constructive criticism to make the manuscript even better.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
We declared that none of the authors have any conflict of interest.
Rights and permissions
About this article
Cite this article
Chattopadhyay, P., Banerjee, G. Recent advancement on chemical arsenal of Bt toxin and its application in pest management system in agricultural field. 3 Biotech 8, 201 (2018). https://doi.org/10.1007/s13205-018-1223-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-018-1223-1