Skip to main content

Bacillus thuringiensis: a successful insecticide with new environmental features and tidings

Abstract

Bacillus thuringiensis (Bt) is known as the most successful microbial insecticide against different orders of insect pests in agriculture and medicine. Moreover, Bt toxin genes also have been efficiently used to enhance resistance to insect pests in genetically modified crops. In light of the scientific advantages of new molecular biology technologies, recently, some other new potentials of Bt have been explored. These new environmental features include the toxicity against nematodes, mites, and ticks, antagonistic effects against plant and animal pathogenic bacteria and fungi, plant growth-promoting activities (PGPR), bioremediation of different heavy metals and other pollutants, biosynthesis of metal nanoparticles, production of polyhydroxyalkanoate biopolymer, and anticancer activities (due to parasporins). This review comprehensively describes recent advances in the Bt whole-genome studies, the last updated known Bt toxins and their functions, and application of cry genes in plant genetic engineering. Moreover, the review thoroughly describes the new features of Bt which make it a suitable cell factory that might be used for production of different novel valuable bioproducts.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Abdelmalek N, Sellami S, Ben Kridis A, Tounsi S, Rouis S (2015) Molecular characterisation of Bacillus thuringiensis strain MEB4 highly toxic to the Mediterranean flour moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Pest Manag Sci. doi:10.1002/ps.4066

    PubMed  Google Scholar 

  • Aceves-Diez AE, Estrada-Castañeda KJ, Castañeda-Sandoval LM (2015) Use of Bacillus thuringiensis supernatant from a fermentation process to improve bioremediation of chlorpyrifos in contaminated soils. J Environ Manag 157:213–219. doi:10.1016/j.jenvman.2015.04.026

    CAS  Article  Google Scholar 

  • Ahern M, Verschueren S, Van Sinderen D (2003) Isolation and characterisation of a novel bacteriocin produced by Bacillus thuringiensis strain B439. FEMS Microbiol Let 220:127–131. doi:10.1016/S0378-1097(03)00086-7

    CAS  Article  Google Scholar 

  • Ahmed N, Wang M, Shu S (2016) Effect of commercial Bacillus thuringiensis toxins on Tyrophagus putrescentiae (Schrank) fed on wolfberry (Lycium barbarum L.). Int J Acarol 42:1–6. doi:10.1080/01647954.2015.1109707

    Article  Google Scholar 

  • Akram W, Mahboob A, Javed AA (2013) Bacillus thuringiensis strain 199 can induce systemic resistance in tomato against Fusarium wilt. Eur J Microbiol Immunol 3:275–280. doi:10.1556/EuJMI.3.2013.4.7

    Article  Google Scholar 

  • Aldeewan A, Zhang Y, Su L (2014) Bacillus thuringiensis parasporins functions on cancer cells. Int J Pure App Biosci 2:67–74

    Google Scholar 

  • Alquisira-Ramírez EV, Paredes-Gonzalez JR, Hernández-Velázquez VM, Ramírez-Trujillo JA, Peña-Chora G (2014) In vitro susceptibility of Varroa destructor and Apis mellifera to native strains of Bacillus thuringiensis. Apidol 45:707–718. doi:10.1007/s13592-014-0288-z

    Article  CAS  Google Scholar 

  • Ammons DR, Short JD, Bailey J, Hinojosa G, Tavarez L, Salazar M, Rampersad JN (2016) Anti-cancer parasporin toxins are associated with different environments: discovery of two novel parasporin 5-like genes. Curr Microbiol 72:184–189. doi:10.1007/s00284-015-0934-3

    CAS  PubMed  Article  Google Scholar 

  • Armada E, Probanza A, Roldán A, Azcón R (2015a) Native plant growth promoting bacteria Bacillus thuringiensis and mixed or individual mycorrhizal species improved drought tolerance and oxidative metabolism in Lavandula dentata plants. J Plant Physiol 192:1–12. doi:10.1016/j.jplph.2015.11.007

    PubMed  Article  CAS  Google Scholar 

  • Armada E, Azcon R, Lopez-Castillo OM, Calvo-Polanco M, Ruiz-Lozano JM (2015b) Autochthonous arbuscular mycorrhizal fungi and Bacillus thuringiensis from a degraded Mediterranean area can be used to improve physiological traits and performance of a plant of agronomic interest under drought conditions. Plant Physiol Biochem 90:64–74. doi:10.1016/j.plaphy.2015.03.004

    CAS  PubMed  Article  Google Scholar 

  • Babu AG, Kim JD, Oh BT (2013) Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J Hazard Mater 250:477–483. doi:10.1016/j.jhazmat.2013.02.014

    PubMed  Article  CAS  Google Scholar 

  • Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781. doi:10.2135/cropsci2003.1774

    Article  Google Scholar 

  • Banu AN, Balasubramanian C, Moorthi PV (2014) Biosynthesis of silver nanoparticles using Bacillus thuringiensis against dengue vector, Aedes aegypti (Diptera: Culicidae). Parasitol Res 113:311–316. doi:10.1007/s00436-013-3656-0

    PubMed  Article  Google Scholar 

  • Barbosa LC, Farias DL, Silva ID, Melo FL, Ribeiro BM, Aguiar RW (2015) Draft genome sequence of Bacillus thuringiensis 147, a Brazilian strain with high insecticidal activity. Mem Inst Oswaldo Cruz 110:822–823. doi:10.1590/0074-02760150273

    PubMed  PubMed Central  Article  Google Scholar 

  • Barboza-Corona JE, Vázquez-Acosta H, Bideshi DK, Salcedo-Hernández R (2007) Bacteriocin-like inhibitor substances produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol 187:117–126

    CAS  PubMed  Article  Google Scholar 

  • Barboza-Corona JE, Vázquez-Acosta H, Bideshi DK, Salcedo-Hernández R (2009) Activity of bacteriocins synthesized by Bacillus thuringiensis against Staphylococcus aureus isolates associated to bovine mastitis. Veter Microbiol 138:179–183. doi:10.1007/s00203-006-0178-5

    CAS  Article  Google Scholar 

  • BCC Research Report (2015) Biopesticides: The Global Market. CHM029E

  • Blackburn MB, Martin PA, Kuhar D, Farrar RR Jr, Gundersen-Rindal DE (2013) Phylogenetic distribution of phenotypic traits in Bacillus thuringiensis determined by multilocus sequence analysis. PLoS One 8:e66061. doi:10.1371/journal.pone.0066061

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bora LC, Kataki L, Talukdar K, Nath BC, Sarkar R (2015) Molecular characterizations of microbial antagonists and development of bioformulations for management of bacterial wilt of Naga chilli (Capsicum chinens jacq.) in Assam. J Exp Biol 3:2

    Google Scholar 

  • Brar SK, Verma M, Tyagi RD, Valéro JR, Surampalli RY (2009) Concurrent degradation of dimethyl phthalate (DMP) during production of Bacillus thuringiensis based biopesticides. J Hazard Mater 171:1016–1023. doi:10.1016/j.jhazmat.2009.06.108

    CAS  PubMed  Article  Google Scholar 

  • Brasseur K, Auger P, Asselin E, Parent S, Côté JC, Sirois M (2015) Parasporin-2 from a new Bacillus thuringiensis 4r2 strain induces caspases activation and apoptosis in human cancer cells. PLoS One 10:e0135106. doi:10.1371/journal.pone.0135106

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Brookes G, Barfoot P (2015) Environmental impacts of genetically modified (GM) crop use 1996–2013: impacts on pesticide use and carbon emissions. GM Crops Food 6:103–133. doi:10.1080/21645698.2015.1025193

    PubMed  PubMed Central  Article  Google Scholar 

  • Challacombe JF, Altherr MR, Xie G, Bhotika SS, Brown N, Bruce D, Campbell CS, Campbell ML, Chen J, Chertkov O, Cleland C (2007) The complete genome sequence of Bacillus thuringiensis Al Hakam. J Bacteriol 189:3680–3681. doi:10.1128/JB.00241-07

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chehimi S, Limam F, Lanneluc I, Delalande F, van Dorsselaer A, Sable S (2012) Identification of three novel B thuringiensis strains that produce the Thuricin S bacteriocin. Bt Res 3(1). doi:10.5376/bt.2012.03.0002

  • Chen S, Deng Y, Chang C, Lee J, Cheng Y, Cui Z, Zhou J, He F, Hu M, Zhang LH (2015a) Pathway and kinetics of cyhalothrin biodegradation by Bacillus thuringiensis strain ZS-19. Sci Rep 5. doi:10.1038/srep08784

  • Chen Z, Chen H, Pan X, Lin Z, Guan X (2015b) Investigation of methylene blue biosorption and biodegradation by Bacillus thuringiensis 016. Water Air Soil Poll 226:1–8. doi:10.1007/s11270-015-2417-3

    Google Scholar 

  • Chen Z, Pan X, Chen H, Lin Z, Guan X (2015c) Investigation of lead (II) uptake by Bacillus thuringiensis 016. World J Microbiol Biotechnol 31:1729–1736. doi:10.1007/s11274-015-1923-1

    CAS  PubMed  Article  Google Scholar 

  • Cherif A, Ouzari H, Daffonchio D, Cherif H, Ben Slama K, Hassen A, Jaoua S (2001) Thuricin 7: a novel bacteriocin produced by Bacillus thuringiensis BMG1 7, a new strain isolated from soil. Lett Appl Microbiol 32:243–247. doi:10.1046/j.1472-765X.2001.00898.x

    CAS  PubMed  Article  Google Scholar 

  • Cherif A, Rezgui W, Raddadi N, Daffonchio D, Boudabous A (2008) Characterization and partial purification of entomocin 110, a newly identified bacteriocin from Bacillus thuringiensis subsp Entomocidus HD110. Microbiol Res 163:684–692. doi:10.1016/j.micres.2006.10.005

    CAS  PubMed  Article  Google Scholar 

  • Cherif-Silini H, Silini A, Yahiaoui B, Ouzari I, Boudabous A (2016) Phylogenetic and plant-growth-promoting characteristics of Bacillus isolated from the wheat rhizosphere. Ann Microbiol:1–11. doi:10.1007/s13213-016-1194-6

  • Chitwood DJ (2003) Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Manag Sci 59:748–753. doi:10.1002/ps.684

    CAS  PubMed  Article  Google Scholar 

  • Craig W, Tepfer M, Degrassi G, Ripandelli D (2008) An overview of general features of risk assessments of genetically modified crops. Euphytica 164:853–880

    Article  Google Scholar 

  • Crickmore N, Zeigler DR, Feitelson J (2016) Bacillus thuringiensis Toxin Nomenclature http://wwwlifescisussexacuk/Home/Neil_Crickmore/Bt/ (Accessed on June, 2016)

  • Das VL, Thomas R, Varghese RT, Soniya EV, Mathew J, Radhakrishnan EK (2014b) Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech 4:121–126. doi:10.1007/s13205-013-0130-8

    PubMed  Article  Google Scholar 

  • Das P, Sinha S, Mukherjee SK (2014a) Nickel bioremediation potential of Bacillus thuringiensis KUNi1 and some environmental factors in nickel removal. Biorem J 18:169–177. doi:10.1080/10889868.2014.889071

    CAS  Article  Google Scholar 

  • Dash HR, Mangwani N, Das S (2014) Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Poll Res 21:2642–2653. doi:10.1007/s11356-013-2206-8

    CAS  Article  Google Scholar 

  • Dave SR, Dave RH (2009) Isolation and characterization of Bacillus thuringiensis for acid red 119 dye decolourisation. Bioresource Technol 100:249–253. doi:10.1016/j.biortech.2008.05.019

    CAS  Article  Google Scholar 

  • de la Fuente-Salcido N, Alanís-Guzmán MG, Bideshi DK, Salcedo-Hernández R, Bautista-Justo M, Barboza-Corona JE (2008) Enhanced synthesis and antimicrobial activities of bacteriocins produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol 190:633–640

    PubMed  Article  CAS  Google Scholar 

  • de la Fuente-Salcido NM, Casados-Vázquez LE, Barboza-Corona JE (2013) Bacteriocins of Bacillus thuringiensis can expand the potential of this bacterium to other areas rather than limit its use only as microbial insecticide. Canad J Microbiol 59:515–522. doi:10.1139/cjm-2013-0284

    Article  CAS  Google Scholar 

  • Devidas P, Rehberger LA (1992) The effects of exotoxin (thuringiensin) from Bacillus thuringiensis on Meloidogyne incognita and Caenorhabditis elegans. Plant Soil 145:115–120. doi:10.1007/BF00009547

    CAS  Article  Google Scholar 

  • 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 Announc 1:e01023–e01013. doi:10.1128/genomeA.01023-13

    PubMed  PubMed Central  Article  Google Scholar 

  • Dong YH, Zhang XF, Xu JL, Zhang LH (2004) Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl Environ Microbiol 70:954–960. doi:10.1128/AEM.70.2.954-960.2004

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Dong Z, Li J, Zheng J, Geng C, Peng D, Sun M (2016) Complete genome sequence of Bacillus thuringiensis CTC—a typical strain with high production of S-layer proteins. J Biotechnol 220:100–101. doi:10.1016/j.jbiotec.2015.12.027

    CAS  PubMed  Article  Google Scholar 

  • Dubois T, Faegri K, Perchat S, Lemy C, Buisson C, Nielsen-LeRoux C, Gohar M, Jacques P, Ramarao N, Kolstø AB, Lereclus D (2012) Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog 8:e1002629. doi:10.1371/journal.ppat.1002629

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Dunstand-Guzmán E, Peña-Chora G, Hallal-Calleros C, Pérez-Martínez M, Hernández-Velazquez VM, Morales-Montor J, Flores-Pérez FI (2015) Acaricidal effect and histological damage induced by Bacillus thuringiensis protein extracts on the mite Psoroptes cuniculi. Parasit Vectors 8:1. doi:10.1186/s13071-015-0890-6

    Article  CAS  Google Scholar 

  • Ekino K, Okumura S, Ishikawa T, Kitada S, Saitoh H, Akao T, Oka T, Nomura Y, Ohba M, Shin T, Mizuki E (2014) Cloning and characterization of a unique cytotoxic protein parasporin-5 produced by Bacillus thuringiensis A1100 strain. Toxins 6:1882–1895. doi:10.3390/toxins6061882

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • El-Sersy NA (2007) Bioremediation of methylene blue by Bacillus thuringiensis 4 G 1: application of statistical designs and surface plots for optimization. Biotechnol 6:34–39

    CAS  Article  Google Scholar 

  • Elsharkawy MM, Nakatani M, Nishimura M, Arakawa T, Shimizu M, Hyakumachi M (2015) Control of tomato bacterial wilt and root-knot diseases by Bacillus thuringiensis CR-371 and Streptomyces avermectinius NBRC14893. Acta Agri Scandinavica, Section B—Soil Plant Sci 65:575–580. doi:10.1080/09064710.2015.1031819

    CAS  Google Scholar 

  • Erban T, Nesvorna M, Erbanova M, Hubert J (2009) Bacillus thuringiensis var tenebrionis control of synanthropic mites (Acari: Acaridida) under laboratory conditions. Exp App Acarol 49:339–346. doi:10.1007/s10493-009-9265-z

    CAS  Article  Google Scholar 

  • Ferreira L, Rosales E, Danko AS, Sanromán MA, Pazos MM (2016) Bacillus thuringiensis a promising bacterium for degrading emerging pollutants. Process Saf Environ Prot 101:19–26. doi:10.1016/j.psep.2015.05.003

    CAS  Article  Google Scholar 

  • Franco-Molina MA, Mendoza-Gamboa E, Roman-Calderon ME, Zapata-Benavides P, Rivera-Morales LG, Zapata-Monsivais L, Coronado-Cerda EE, Sierra-Rivera CA, Tamez-Guerra R, Rodriguez-Padilla C (2016) In vitro antitumoral activity of soluble protein extracts of Bacillus thuringiensis. Afr J Microbiol Res 10:324–329. doi:10.5897/AJMR2015.7551

    CAS  Article  Google Scholar 

  • Gao X, Han Q, Chen Y, Qin H, Huang L, Kang Z (2014) Biological control of oilseed rape Sclerotinia stem rot by Bacillus subtilis strain Em7. Biocontrol Sci Tech 24:39–52. doi:10.1080/09583157.2013.844223

    Article  Google Scholar 

  • Gao Q, Zheng J, Zhu L, Ruan L, Peng D, Sun M (2015) Complete genome sequence of Bacillus thuringiensis tenebrionis 4AA1, a typical strain with toxicity to Coleopteran insects. J Biotechnol 204:15–16. doi:10.1016/j.jbiotec.2015.03.009

    CAS  PubMed  Article  Google Scholar 

  • Gomaa EZ (2012) Chitinase production by Bacillus thuringiensis and Bacillus licheniformis: their potential in antifungal biocontrol. J Microbiol 50:103–111. doi:10.1007/s12275-012-1343-y

    CAS  PubMed  Article  Google Scholar 

  • Guan P, Ai P, Dai X, Zhang J, Xu L, Zhu J, Li Q, Deng Q, Li S, Wang S, Liu H (2012) Complete genome sequence of Bacillus thuringiensis serovar Sichuansis strain MC28. J Bacteriol 194:6975–6975. doi:10.1128/JB.01861-12

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Guo S, Liu M, Peng D, Ji S, Wang P, Yu Z, Sun M (2008) New strategy for isolating novel nematicidal crystal protein genes from Bacillus thuringiensis strain YBT-518. Appl Environ Microbiol 74:6997–7001. doi:10.1128/AEM.01346-08

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, Zeng G, Liu C, Wan Y, Chen J, He Y (2010) Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp L14. Bioresource Technol 101:8599–8605. doi:10.1016/j.biortech.2010.06.085

    CAS  Article  Google Scholar 

  • Gutiérrez-Chávez AJ, Martínez-Ortega EA, Valencia-Posadas M, León-Galván MF, de la Fuente-Salcido NM, Bideshi DK, Barboza-Corona JE (2016) Potential use of Bacillus thuringiensis bacteriocins to control antibiotic-resistant bacteria associated with mastitis in dairy goats. Folia Microbiol 61:11–19. doi:10.1007/s12223-015-0404-0

    Article  CAS  Google Scholar 

  • Han CS, Xie G, Challacombe JF, Altherr MR, Bhotika SS, Bruce D, Campbell CS, Campbell ML, Chen J, Chertkov O, Cleland C (2006) Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J Bacteriol 188:3382–3390. doi:10.1128/JB.188.9.3382-3390.2006

    PubMed  PubMed Central  Article  Google Scholar 

  • Hassanain MA, Garhy ME, Abdel-Ghaffar FA, El-Sharaby A, Megeed KN (1997) Biological control studies of soft and hard ticks in Egypt I the effect of Bacillus thuringiensis varieties on soft and hard ticks (Ixodidade). Parasitol Res 83:209213

    CAS  PubMed  Article  Google Scholar 

  • Hassen A, Saidi N, Cherif M, Boudabous A (1998) Effects of heavy metals on Pseudomonas aeruginosa and Bacillus thuringiensis. Bioresource Technol 65:73–82. doi:10.1016/S0960-8524(98)00011-X

    CAS  Article  Google Scholar 

  • Hayakawa T, Kanagawa R, Kotani Y, Kimura M, Yamagiwa M, Yamane Y, Takebe S, Sakai H (2007) Parasporin-2Ab, a newly isolated cytotoxic crystal protein from Bacillus thuringiensis. Curr Microbiol 55:278–283. doi:10.1007/s00284-006-0351-8

    CAS  PubMed  Article  Google Scholar 

  • He J, Shao X, Zheng H, Li M, Wang J, Zhang Q, Li L, Liu Z, Sun M, Wang S, Yu Z (2010) Complete genome sequence of Bacillus thuringiensis mutant strain BMB171. J Bacteriol 192:4074–4075. doi:10.1128/JB.00562-10

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • He J, Wang J, Yin W, Shao X, Zheng H, Li M, Zhao Y, Sun M, Wang S, Yu Z (2011) Complete genome sequence of Bacillus thuringiensis subsp chinensis strain CT-43. J Bacteriol 193:3407–3408. doi:10.1128/JB.05085-11

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Hong CE, Jo SH, Moon JY, Lee JS, Kwon SY, Park JM (2015) Isolation of novel leaf-inhabiting endophytic bacteria in Arabidopsis thaliana and their antagonistic effects on phytophathogens. Plant Biotechnol Rep 9:451–458. doi:10.1007/s11816-015-0372-5

    Article  Google Scholar 

  • Hu Y, Aroian RV (2012) Promise of Bacillus thuringiensis crystal proteins as Anthelmintics. Parasitic Helminths: Targets, Screens, Drugs and Vaccines:267–281. doi:10.1002/9783527652969.ch16

  • Huang J, Ye J, Ma J (2014a) Triphenyltin biosorption, dephenylation pathway and cellular responses during triphenyltin biodegradation by Bacillus thuringiensis and tea saponin. Chem Eng J 249:167–173 dx.doi.org/10.1016/j.cej.2014.03.110

    CAS  Article  Google Scholar 

  • Huang TP, Ying XI, Jie-Ru PA, Zhi CH, Li-Fen LI, Lei XU, Zhang LL, Xiong GU (2014b) Aerobic Cr (VI) reduction by an indigenous soil isolate Bacillus thuringiensis BRC-ZYR2. Pedosphere 24:652–661. doi:10.1016/S1002-0160(14)60051-5

    Article  Google Scholar 

  • Iatsenko I, Boichenko I, Sommer RJ (2014a) Bacillus thuringiensis DB27 produces two novel protoxins, Cry21Fa1 and Cry21Ha1, which act synergistically against nematodes. Appl Environ Microbiol 80:3266–3275. doi:10.1128/AEM.00464-14

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Iatsenko I, Corton C, Pickard DJ (2014b) Draft genome sequence of highly nematicidal Bacillus thuringiensis DB27. Genome Announc 2:e00101–e00114. doi:10.1128/genomeA.00101-14

    PubMed  PubMed Central  Article  Google Scholar 

  • ISAAA’s GM Approval Database, 2016 http://wwwisaaaorg/gmapprovaldatabase/

  • Jahan N, Idrees M, Zahid MT, Ali NM, Hussain M (2016) Molecular identification and characterization of heavy metal resistant bacteria and their role in bioremediation of chromium. British Microbiol Res J 13(6)

  • Jain D, Kachhwaha S, Jain R, Srivastava G, Kothari SL (2010) Novel microbial route to synthesize silver nanoparticles using spore crystal mixture of Bacillus thuringiensis. Indian J Exp Biol 48:1152 http://imsear.hellis.org/handle/123456789/145076

    CAS  PubMed  Google Scholar 

  • Jain D, Saharan V, Pareek S (2016) Current status of Bacillus thuringiensis: insecticidal crystal proteins and transgenic crops in advances in plant breeding strategies: agronomic, abiotic and biotic stress traits (657–698). Springer International Publishing, New York. doi:10.1007/978-3-319-22518-0_18

    Google Scholar 

  • James C (2015) Global Status of Commercialized Biotech/GM Crops: 2015 ISAAA Brief No 51 ISAAA: Ithaca, NY. http://www.isaaa.org/resources/publications/annualreport/2015/default.asp

  • Jeong H, Jo SH, Hong CE, Park JM (2016) Genome sequence of the endophytic bacterium Bacillus thuringiensis strain KB1, a potential biocontrol agent against phytopathogens. Genome Announc 4:e00279–e00216. doi:10.1128/genomeA.00279-16

    PubMed  PubMed Central  Google Scholar 

  • Jisha VN, Smitha RB, Benjamin S (2013) An overview on the crystal toxins from Bacillus thuringiensis. Adv Microbiol 3(05):462. doi:10.4236/aim.2013.35062

    CAS  Article  Google Scholar 

  • Johnson SL, Daligault HE, Davenport KW, Jaissle J, Frey KG, Ladner JT, Broomall SM, Bishop-Lilly KA, Bruce DC, Gibbons HS, Coyne SR (2015) Complete genome sequences for 35 biothreat assay-relevant Bacillus species. Genome Announc 3:e00151–e00115. doi:10.1128/genomeA.00151-15

    PubMed  PubMed Central  Google Scholar 

  • Juibari MM, Yeganeh LP, Abbasalizadeh S, Azarbaijani R, Mousavi SH, Tabatabaei M, Jouzani GS, Salekdeh GH (2011) Intensified biosynthesis of silver nanoparticles using a native extremophilic Ureibacillus thermosphaericus strain. Mater Let 65:1014–1017. doi:10.1007/s12668-015-0185-6

    CAS  Article  Google Scholar 

  • Juibari MM, Yeganeh LP, Abbasalizadeh S, Azarbaijani R, Mousavi SH, Tabatabaei M, Jouzani GS, Salekdeh GH (2015) Investigation of a hot-spring extremophilic Ureibacillus thermosphaericus strain Thermo-BF for extracellular biosynthesis of functionalized gold nanoparticles. BioNanoSci 5:233–241. doi:10.1007/s12668-015-0185-6

    Article  Google Scholar 

  • Kamoun F, Fguira IB, Hassen NB, Mejdoub H, Lereclus D, Jaoua S (2011) Purification and characterization of a new Bacillus thuringiensis bacteriocin active against Listeria monocytogenes, Bacillus cereus and Agrobacterium tumefaciens. Appl Biochem Biotechnol 165:300–314. doi:10.1007/s12010-011-9252-9

    CAS  PubMed  Article  Google Scholar 

  • Kanda K, Nakashima K, Nagano Y (2015) Complete genome sequence of Bacillus thuringiensis serovar tolworthi strain Pasteur Institute Standard. Genome Announc 3:e00710–e00715. doi:10.1128/genomeA.00710-15

    PubMed  PubMed Central  Article  Google Scholar 

  • Katayama H, Yokota H, Akao T, Nakamura O, Ohba M, Mekada E, Mizuki E (2005) Parasporin-1, a novel cytotoxic protein to human cells from non-insecticidal parasporal inclusions of Bacillus thuringiensis. J Biochem 137:17–25. doi:10.1093/jb/mvi003

    CAS  PubMed  Article  Google Scholar 

  • Kebria DY, Khodadadi A, Ganjidoust H, Badkoubi A, Amoozegar MA (2009) Isolation and characterization of a novel native Bacillus strain capable of degrading diesel fuel. Int J Environ Sci Technol 6:435–442. doi:10.1007/BF03326082

    CAS  Article  Google Scholar 

  • Khan MQ, Abbasi MW, Zaki MJ, Khan SA (2010) Evaluation of Bacillus thuringiensis isolates against root-knot nematodes following seed application in okra and mungbean. Pakistan J Botany 42:2903–2910

    Google Scholar 

  • Kim PI, Bai H, Bai D, Chae H, Chung S, Kim Y, Park R, Chi YT (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97:942–949. doi:10.1111/j.1365-2672.2004.02356.x

    CAS  PubMed  Article  Google Scholar 

  • Kotze AC, O’grady J, Gough JM, Pearson R, Bagnall NH, Kemp DH, Akhurst RJ (2005) Toxicity of Bacillus thuringiensis to parasitic and free-living life-stages of nematode parasites of livestock. Int J Parasitol 35:1013–1022. doi:10.1016/j.ijpara.2005.03.010

    CAS  PubMed  Article  Google Scholar 

  • Krishnan K, Ker JE, Mohammed SM, Nadarajah VD (2010) Identification of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) as a binding protein for a 68-kDa Bacillus thuringiensis parasporal protein cytotoxic against leukaemic cells. J Biomed Sci 17:86. doi:10.1186/1423-0127-17-86

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Kumar P, Chandra R (2004) Detoxification of distillery effluent through Bacillus thuringiensis (MTCC 4714) enhanced phytoremediation potential of Spirodela polyrrhiza (L) Schliden Bull Environ Contam. Toxicol 73:903–910. doi:10.1007/s00128-004-0512-z

    CAS  Google Scholar 

  • Kumar P, Chandra R (2006) Decolourisation and detoxification of synthetic molasses melanoidins by individual and mixed cultures of Bacillus spp. Bioresource Technol 97:2096–2102. doi:10.1016/j.biortech.2005.10.012

    CAS  Article  Google Scholar 

  • Kumar V, Singh S, Kashyap N, Singla S, Bhadrecha P, Kaur P (2015) Bioremediation of heavy metals by employing resistant microbial isolates from agricultural soil irrigated with industrial waste water. Oriental J Chem 31:357–361

  • Lacey LA, Frutos R, Kaya HK, Vail P (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41. doi:10.1006/bcon.2001.0938

    CAS  PubMed  Article  Google Scholar 

  • Lecadet MM (2013) Bacillus thuringiensis toxins—the proteinaceous crystal. Bacterial Protein Toxins 3:437–471

    Google Scholar 

  • Lecadet MM, Frachon E, Dumanoir VC, Ripouteau H, Hamon S, Laurent P, Thiery I (1999) Updating the H-antigen classification of Bacillus thuringiensis. J Appl Microbiol 86:660–672. doi:10.1046/j.1365-2672.1999.00710.x

    CAS  PubMed  Article  Google Scholar 

  • Lee KD, Gray EJ, Mabood F, Jung WJ, Charles T, Clark SR, Ly A, Souleimanov A, Zhou X, Smith DL (2009) The class IId bacteriocin thuricin-17 increases plant growth. Planta 229:747–755. doi:10.1007/s00425-008-0870-6

  • Li XQ, Wei JZ, Tan A, Aroian RV (2007) Resistance to root-knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant Biotechnol J 5:455–464

    CAS  PubMed  Article  Google Scholar 

  • Li XQ, Tan A, Voegtline M, Bekele S, Chen CS, Aroian RV (2008) Expression of Cry5B protein from Bacillus thuringiensis in plant roots confers resistance to root-knot nematode. Biol Control 47:97–102

    Article  CAS  Google Scholar 

  • Li Q, Zou T, Ai P, Pan L, Fu C, Li P, Zheng A (2015a) Complete genome sequence of Bacillus thuringiensis HS18-1. J Biotechnol 214:61–62

    CAS  PubMed  Article  Google Scholar 

  • Li Q, Xu LZ, Zou T, Ai P, Huang GH, Li P, Zheng AP (2015b) Complete genome sequence of Bacillus thuringiensis strain HD521 Standards. Genomic Sci 10:1. doi:10.1186/s40793-015-0058-1

    Article  CAS  Google Scholar 

  • Liu G, Song L, Shu C, Wang P, Deng C, Peng Q, Lereclus D, Wang X, Huang D, Zhang J, Song F (2013) Complete genome sequence of Bacillus thuringiensis subsp kurstaki strain HD73. Genome Announc 1:e00080–e00013. doi:10.1128/genomeA.00080-13

    PubMed  Google Scholar 

  • Luo H, Xiong J, Zhou Q, Xia L, Yu Z (2013a) The effects of Bacillus thuringiensis Cry6A on the survival, growth, reproduction, locomotion, and behavioral response of Caenorhabditis elegans. Appl Microbiol Biotechnol 97:10135–10142. doi:10.1007/s00253-013-5249-3

    CAS  PubMed  Article  Google Scholar 

  • Luo X, Chen L, Huang Q, Zheng J, Zhou W, Peng D, Ruan L, Sun M (2013b) Bacillus thuringiensis metalloproteinase Bmp1 functions as a nematicidal virulence factor. Appl Environ Microbiol 79:460–468. doi:10.1128/AEM.02551-12

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Maiti A, Das S, Bhattacharyya N (2012) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons by Bacillus thuringiensis strain NA2. J Sci 1:72–75 www.worldsciencepublisher.org

    Google Scholar 

  • Mandal K, Singh B, Jariyal M, Gupta VK (2013) Microbial degradation of fipronil by Bacillus thuringiensis. Ecotoxicol Environ Saf 93:87–92. doi:10.1016/j.ecoenv.2013.04.001

    CAS  PubMed  Article  Google Scholar 

  • Marimuthu S, Rahuman AA, Kirthi AV, Santhoshkumar T, Jayaseelan C, Rajakumar G (2013) Eco-friendly microbial route to synthesize cobalt nanoparticles using Bacillus thuringiensis against malaria and dengue vectors. Parasitol Res 112:4105–4112. doi:10.1007/s00436-013-3601-2

    PubMed  Article  Google Scholar 

  • Martínez-Absalón S, Rojas-Solís D, Hernández-León R, Prieto-Barajas C, Orozco-Mosqueda MD, Peña-Cabriales JJ, Sakuda S, Valencia-Cantero E, Santoyo G (2014) Potential use and mode of action of the new strain Bacillus thuringiensis UM96 for the biological control of the grey mould phytopathogen Botrytis cinerea. Biocontrol Sci Tech 24:1349–1362. doi:10.1080/09583157.2014.940846

    Article  Google Scholar 

  • Melo AL, Soccol VT, Soccol CR (2016) Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Critical Rev Biotechnol 36:317–326. doi:10.3109/07388551.2014.960793

    CAS  Article  Google Scholar 

  • Mishra PK, Mishra S, Selvakumar G, Bisht JK, Kundu S, Gupta HS (2009a) Coinoculation of Bacillus thuringeinsis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L) and lentil (Lens culinaris L). World J Microbiol Biotechnol 25:753–761. doi:10.1007/s11274-009-9963-z

    Article  Google Scholar 

  • Mishra PK, Mishra S, Selvakumar G, Kundu S, Shankar Gupta H (2009b) Enhanced soybean (Glycine max L) plant growth and nodulation by Bradyrhizobium japonicum-SB1 in presence of Bacillus thuringiensis-KR1. Acta Agric Scand Section B–Soil and Plant Sci 59:189–196. doi:10.1080/09064710802040558

    CAS  Google Scholar 

  • Mizuki E, Ohba M, Akao T, Yamashita S, Saitoh H, Park YS (1999) Unique activity associated with non-insecticidal Bacillus thuringiensis parasporal inclusions: in vitro cell-killing action on human cancer cells. J Appl Microbiol 86:477–486. doi:10.1046/j.1365-2672.1999.00692.x

    CAS  PubMed  Article  Google Scholar 

  • Mohammed SH, El Saedy MA, Enan MR, Ibrahim NE, Ghareeb A, Moustafa SA (2008) Biocontrol efficiency of Bacillus thuringiensis toxins against root-knot nematode, Meloidogyne incognita. J Cell Mol Biol 7:57–66 http://jcmb.halic.edu.tr

    Google Scholar 

  • Murawska E, Fiedoruk K, Bideshi DK, Swiecicka I (2013) Complete genome sequence of Bacillus thuringiensis subsp thuringiensis strain IS5056, an isolate highly toxic to Trichoplusia ni. Genome Announc 1:e00108–e00113. doi:10.1128/genomeA.00108-13

    PubMed Central  Article  Google Scholar 

  • Nayak PS, Arakha M, Kumar A, Asthana S, Mallick BC, Jha S (2016) An approach towards continuous production of silver nanoparticles using Bacillus thuringiensis. RSC Adv 6:8232–8242. doi:10.1039/C5RA21281B

    CAS  Article  Google Scholar 

  • Nazarian A, Jahangiri R, Salehi Jouzani G, Seifinejad A, Soheilivand S, Bagheri O, Keshavarzi M, Alamisaeid K (2009) Coleopteran-specific and putative novel cry genes in Iranian native Bacillus thuringiensis collection. J Invertebr Pathol 102:101–109. doi:10.1016/j.jip.2009.07.009

    CAS  PubMed  Article  Google Scholar 

  • Neethu KB, Priji P, Unni KN, Sajith S, Sreedevi S, Ramani N, Anitha K, Rosana B, Girish MB, Benjamin S (2016) New Bacillus thuringiensis strain isolated from the gut of Malabari goat is effective against Tetranychus macfarlanei. J Appl Entomol 140:187–198. doi:10.1111/jen.12235

    Article  Google Scholar 

  • Ohba M, Mizuki E, Uemori A (2009) Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Res 29:427–433 http://ar.iiarjournals.org/content/29/1/427.short

    CAS  PubMed  Google Scholar 

  • Okafor F, Janen A, Kukhtareva T, Edwards V, Curley M (2013) Green synthesis of silver nanoparticles, their characterization, application and antibacterial activity. Int J Environ Res Public Health 10:5221–5238. doi:10.3390/ijerph10105221

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Okumura S, Saitoh H, Ishikawa T, Wasano N, Yamashita S, Kusumoto KI, Akao T, Mizuki E, Ohba M, Inouye K (2005) Identification of a novel cytotoxic protein, Cry45Aa, from Bacillus thuringiensis A1470 and its selective cytotoxic activity against various mammalian cell lines. J Agric Food Chem 53:6313–6318. doi:10.1021/jf0506129

    CAS  PubMed  Article  Google Scholar 

  • Okumura S, Saitoh H, Ishikawa T, Inouye K, Mizuki E (2011) Mode of action of parasporin-4, a cytocidal protein from Bacillus thuringiensis. BBA Biomemb 1808:1476–1482. doi:10.1016/j.bbamem.2010.11.003

    CAS  Article  Google Scholar 

  • Olukanni OD, Adenopo A, Awotula AO, Osuntoki AA (2013) Biodegradation of malachite green by extracellular laccase producing Bacillus thuringiensis RUN1. J Basic Appl Sci 9:543

    Google Scholar 

  • Ortiz N, Armada E, Duque E, Roldán A, Azcón R (2015) Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J Plant Physiol 174:87–96. doi:10.1016/j.jplph.2014.08.019

    CAS  PubMed  Article  Google Scholar 

  • Oves M, Khan MS, Zaidi A (2013) Biosorption of heavy metals by Bacillus thuringiensis strain OSM29 originating from industrial effluent contaminated north Indian soil. Saudi J Biol Sci 20:121–129. doi:10.1016/j.sjbs.2012.11.006

    CAS  PubMed  Article  Google Scholar 

  • Paik HD, Bae SS, Park SH, Pan JG (1997) Identification and partial characterization of tochicin, a bacteriocin produced by Bacillus thuringiensis subsp tochigiensis. J Ind Microbiol Biotechnol 19:294–298. doi:10.1038/sj.jim.2900462

    CAS  PubMed  Article  Google Scholar 

  • Pan X, Chen Z, Chen F, Cheng Y, Lin Z, Guan X (2015) The mechanism of uranium transformation from U (VI) into nano-uramphite by two indigenous Bacillus thuringiensis strains. J Hazard Mater 297:313–319 dx.doi.org/10.1016/j.jhazmat.2015.05.019

    CAS  PubMed  Article  Google Scholar 

  • Pane C, Villecco D, Campanile F, Zaccardelli M (2012) Novel strains of bacillus, isolated fromcompost and compost amended soils, as biological control agents against soil-borne phytopathogenic fungi. Biocontrol Sci Tech 22:1373–1388. doi:10.1080/09583157.2012.729143

    Article  Google Scholar 

  • Park SJ, Park SY, Ryu CM, Park SH, Lee JK (2008) The role of AiiA, a quorum-quenching enzyme from Bacillus thuringiensis, on the rhizosphere competence. J Microbiol Biotechnol 18:1518–1521

    CAS  PubMed  Google Scholar 

  • Peng D, Lin J, Huang Q, Zheng W, Liu G, Zheng J, Zhu L, Sun M (2016) A novel metalloproteinase virulence factor is involved in Bacillus thuringiensis pathogenesis in nematodes and insects. Environ Microbiol. doi:10.1111/1462-2920.13069

    Google Scholar 

  • Periyasamy A, Kkani P, Chandrasekaran B, Ponnusamy S, Viswanathan S, Selvanayagam P, Rajaiah S (2016) Screening and characterization of a non-insecticidal Bacillus thuringiensis strain producing parasporal protein with selective toxicity against human colon cancer cell lines. Ann Microbiol:1–12. doi:10.1007/s13213-016-1204-8

  • Poopathi S, Abidha S (2008) Biodegradation of poultry waste for the production of mosquitocidal toxins. Int Biodeter Biodegr 62:479–482. doi:10.1016/j.ibiod.2008.03.005

    CAS  Article  Google Scholar 

  • Poornima K, Selvanayagam P, Shenbagarathai R (2010) Identification of native Bacillus thuringiensis strain from South India having specific cytocidal activity against cancer cells. J Appl Microbiol 109:348–354. doi:10.1111/j.1365-2672.2010.04697.x

    CAS  PubMed  Google Scholar 

  • Prudent M, Salon C, Souleimanov A, Emery RN, Smith DL (2015) Soybean is less impacted by water stress using Bradyrhizobium japonicum and thuricin-17 from Bacillus thuringiensis. Agron Sustain Dev 35:749–757. doi:10.1007/s13593-014-0256-z

    CAS  Article  Google Scholar 

  • Raybould A (2006) Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops. Environ Biosaf Res 5:119–125

    Article  Google Scholar 

  • Reyes-Ramírez A, Escudero-Abarca BI, Aguilar-Uscanga G, Hayward-Jones PM, Barboza-Corona JE (2004) Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J Food Sci 69:M131–M134. doi:10.1111/j.1365-2621.2004.tb10721.x

    Article  Google Scholar 

  • Rocha LO, Tralamazza SM, Reis GM, Rabinovitch L, Barbosa CB, Corrêa B (2014) Multi-method approach for characterizing the interaction between Fusarium verticillioides and Bacillus thuringiensis subsp kurstaki. PLoS One 9:e92189. doi:10.1371/journal.pone.0092189

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Roy A, Mahata D, Paul D, Korpole S, Franco OL, Mandal SM (2013) Purification, biochemical characterization and self-assembled structure of a fengycin-like antifungal peptide from Bacillus thuringiensis strain SM1. Front Microbiol 4:10–3389. doi:10.3389/fmicb.2013.00332

    Google Scholar 

  • Ruan L, Crickmore N, Peng D, Sun M (2015) Are nematodes a missing link in the confounded ecology of the entomopathogen Bacillus thuringiensis? Trends Microbiol 23:341–346. doi:10.1016/j.tim.2015.02.011

    CAS  PubMed  Article  Google Scholar 

  • Sadfi N, Cherif M, Fliss I, Boudabbous A, Antoun H (2001) Evaluation of bacterial isolates from salty soils and Bacillus thuringiensis strains for the biocontrol of Fusarium dry rot of potato tubers. J Plant Pathol:101–117 http://www.jstor.org/stable/41998046

  • Salehi Jouzani G (2012) Risk assessment of GM crops; challenges in regulations and science. J Biosafety 1:4. doi:10.4172/2167-0331.1000e113

    Google Scholar 

  • Salehi Jouzani G, Abad AP, Seifinejad A, Marzban R, Kariman K, Maleki B (2008a) Distribution and diversity of dipteran-specific cry and cyt genes in native Bacillus thuringiensis strains obtained from different ecosystems of Iran. J Ind Microbiol Biotechnol 35:83–94. doi:10.1007/s10295-007-0269-6

    CAS  Article  Google Scholar 

  • Salehi Jouzani G, Seifinejad A, Saeedizadeh A, Nazarian A, Yousefloo M, Soheilivand S, Mousivand M, Jahangiri R, Yazdani M, Amiri RM, Akbari S (2008b) Molecular detection of nematicidal crystalliferous Bacillus thuringiensis strains of Iran and evaluation of their toxicity on free-living and plant-parasitic nematodes. Canad J Microbiol 54:812–822. doi:10.1139/W08-074

    CAS  Article  Google Scholar 

  • Salehi Jouzani G, Goldenkova IV, Piruzian ES (2008c) Expression of hybrid cry3aM–licBM2 genes in transgenic potatoes (Solanum tuberosum). Plant Cell Tissue Organ Cult 92:321–325. doi:10.1007/s11240-007-9333-1

    CAS  Article  Google Scholar 

  • Sánchez-Soto AI, Saavedra-González GI, Ibarra JE, Salcedo-Hernández R, Barboza-Corona JE, Rincón-Castro D (2015) Detection of β-exotoxin synthesis in Bacillus thuringiensis using an easy bioassay with the nematode Caenorhabditis elegans. Lett Appl Microbiol 61:562–567

    PubMed  Article  CAS  Google Scholar 

  • Santiago TR, Grabowski C, Rossato M, Romeiro RS, Mizubuti ES (2015) Biological control of eucalyptus bacterial wilt with rhizobacteria. Biol Control 80:14–22. doi:10.1016/j.biocontrol.2014.09.007

    Article  Google Scholar 

  • Seifinejad A, Salehi Jouzani G, Hosseinzadeh A, Abdmishani C (2008) Characterization of Lepidoptera-active cry and vip genes in Iranian Bacillus thuringiensis strain collection. Biol Control 44:216–226. doi:10.1016/j.biocontrol.2007.09.010

    CAS  Article  Google Scholar 

  • Sheppard AE, Poehlein A, Rosenstiel P, Liesegang H, Schulenburg H (2013) Complete genome sequence of Bacillus thuringiensis strain 407 Cry. Genome Announc 1:e00158–e00112. doi:10.1128/genomeA.00158-12

    PubMed  PubMed Central  Article  Google Scholar 

  • Shrestha A, Sultana R, Chae JC, Kim K, Lee KJ (2015) Bacillus thuringiensis C25 which is rich in cell wall degrading enzymes efficiently controls lettuce drop caused by Sclerotinia minor. Eur J Plant Pathol 142:577–589. doi:10.1007/s10658-015-0636-5

    CAS  Article  Google Scholar 

  • Singh M, Kumar P, Patel SK, Kalia VC (2013) Production of polyhydroxyalkanoate co-polymer by Bacillus thuringiensis. Indian J Microbiol 53:77–83. doi:10.1007/s12088-012-0294-7

    CAS  PubMed  Article  Google Scholar 

  • Sinott MC, Cunha Filho NA, Castro LL, Lorenzon LB, Pinto NB, Capella GA, Leite FP (2012) Bacillus spp toxicity against Haemonchus contortus larvae in sheep fecal cultures. Exp Parasitol 132:103–108. doi:10.1016/j.exppara.2012.05.015

    CAS  PubMed  Article  Google Scholar 

  • Sukhumungoon P, Rattanachuay P, Hayeebilan F, Kantachote D (2013) Biodegradation of ethidium bromide by Bacillus thuringiensis isolated from soil. Afr J Microbiol Res 7:471–476. doi:10.5897/AJMR12.1642

    CAS  Google Scholar 

  • Surhio MA, Talpur FN, Nizamani SM, Amin F, Bong CW, Lee CW, Ashraf MA, Shah MR (2014) Complete degradation of dimethyl phthalate by biochemical cooperation of the Bacillus thuringiensis strain isolated from cotton field soil. RSC Adv 4:55960–55966. doi:10.1039/C4RA09465D

    CAS  Article  Google Scholar 

  • Tang Y, Zou J, Zhang L, Li Z, Ma C, Ma N (2012) Anti-fungi activities of Bacillus thuringiensis H3 chitinase and immobilized chitinase particles and their effects to rice seedling defensive enzymes. J Nanosci Nanotechnol 12:8081–8086 https://doi.org/10.1166/jnn.2012.6639

    CAS  PubMed  Article  Google Scholar 

  • Tao A, Pang F, Huang S, Yu G, Li B, Wang T (2014) Characterization of endophytic Bacillus thuringiensis strains isolated from wheat plants as biocontrol agents against wheat flag smut. Biocontrol Sci Tech 24:901–924. doi:10.1080/09583157.2014.904502

    Article  Google Scholar 

  • Thamer M, Al-Kubaisi AR, Zahraw Z, Abdullah HA, Hindy I, Khadium A (2013) Biodegradation of Kirkuk light crude oil by Bacillus thuringiensis, Northern of Iraq. Nat Sci 5. doi:10.4236/ns 2013 57104

  • Tohidfar M, Salehi Jouzani G (2008) Genetic engineering of crop plants for enhanced resistance to insects and diseases in Iran. Transgen Plant J 2:151–156

    Google Scholar 

  • Tohidfar M, Zare N, Salehi Jouzani G, Eftekhari SM (2013) Agrobacterium-mediated transformation of alfalfa (Medicago sativa) using a synthetic cry3a gene to enhance resistance against alfalfa weevil. Plant Cell Tissue Organ Cult 113:227–235. doi:10.1007/s11240-012-0262-2

    CAS  Article  Google Scholar 

  • Ugras S, Demirbag Z (2013) Screening antibacterial activity of entomopathogenic bacteria isolated from pests of hazelnut. Biol 68:592–598 https://www.degruyter.com/view/j/biolog.2013.68.issue-4/s11756-013-0210-6/s11756-013-0210-6.xml

    CAS  Google Scholar 

  • Urban JF Jr, Hu Y, Miller MM, Scheib U, Yiu YY, Aroian RV (2013) Bacillus thuringiensis-derived Cry5B has potent anthelmintic activity against Ascaris suum. PLoS Negl Trop Dis 7:e2263. doi:10.1371/journal.pntd.0002263

    PubMed  PubMed Central  Article  Google Scholar 

  • Velivelli SL, De Vos P, Kromann P, Declerck S, Prestwich BD (2014) Biological control agents: from field to market, problems, and challenges. Trends Biotechnol 32:493–496. doi:10.1016/j.tibtech.2014.07.002

    CAS  PubMed  Article  Google Scholar 

  • Wang P, Zhang C, Guo M, Guo S, Zhu Y, Zheng J, Zhu L, Ruan L, Peng D, Sun M (2014) Complete genome sequence of Bacillus thuringiensis YBT-1518, a typical strain with high toxicity to nematodes. J Biotechnol 171:1–2. doi:10.1016/j.jbiotec.2013.11.023

    CAS  PubMed  Article  Google Scholar 

  • Wu S, Peng Y, Huang Z, Huang Z, Xu L, Ivan G, Guan X, Zhang L, Zou S (2015) Isolation and characterization of a novel native Bacillus thuringiensis strain BRC-HZM2 capable of degrading chlorpyrifos. J Basic Microbiol 55:389–397. doi:10.1002/jobm.201300501

    CAS  PubMed  Article  Google Scholar 

  • Yamashita S, Katayama H, Saitoh H, Akao T, Park YS, Mizuki E, Ohba M, Ito A (2005) Typical three-domain Cry proteins of Bacillus thuringiensis strain A1462 exhibit cytocidal activity on limited human cancer cells. J Biochem 138:663–672. doi:10.1093/jb/mvi177

    CAS  PubMed  Article  Google Scholar 

  • Yu Z, Luo H, Xiong J, Zhou Q, Xia L, Sun M, Li L (2014) Bacillus thuringiensis Cry6A exhibits nematicidal activity to Caenorhabditis elegans bre mutants and synergistic activity with Cry5B to C elegans. Lett Appl Microbiol 58:511–519. doi:10.1111/lam.12219

    CAS  PubMed  Article  Google Scholar 

  • Yu Z, Xiong J, Zhou Q, Luo H, Hu S, Xia L, Sun M, Li L, Yu Z (2015) The diverse nematicidal properties and biocontrol efficacy of Bacillus thuringiensis Cry6A against the root-knot nematode Meloidogyne hapla. J Invertebr Pathol 125:73–80. doi:10.1016/j.jip.2014.12.011

    CAS  PubMed  Article  Google Scholar 

  • Zhang F, Peng D, Ye X, Yu Z, Hu Z, Ruan L, Sun M (2012) In vitro uptake of 140 kDa Bacillus thuringiensis nematicidal crystal proteins by the second stage juvenile of Meloidogyne hapla. PLoS One 7:e38534. doi:10.1371/journal.pone.0038534

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang L, Yu J, Xie Y, Lin H, Huang Z, Xu L, Gelbič I, Guan X (2014) Biological activity of Bacillus thuringiensis (Bacillales: Bacillaceae) chitinase against Caenorhabditis elegans (Rhabditida: Rhabditidae). J Econom Entomol 107:551–558. doi:10.1603/EC13201

    CAS  Article  Google Scholar 

  • Zheng M, Shi J, Shi J, Wang Q, Li Y (2013) Antimicrobial effects of volatiles produced by two antagonistic bacillus strains on the anthracnose pathogen in postharvest mangos. Biol Control 65:200–206. doi:10.1016/j.biocontrol.2013.02.004

    CAS  Article  Google Scholar 

  • Zhioua E, Heyer K, Browning M, Ginsberg HS, LeBrun RA (1999) Pathogenicity of Bacillus thuringiensis variety kurstaki to Ixodes scapularis (Acari: Ixodidae). J Med Entomol 36:900902. doi:10.1093/jmedent/36.6.900

    CAS  PubMed  Article  Google Scholar 

  • Zhou M, Yu H, Yin X, Sabour PM, Chen W, Gong J (2014) Lactobacillus zeae protects Caenorhabditis elegans from enterotoxigenic Escherichia coli-caused death by inhibiting enterotoxin gene expression of the pathogen. PLoS One 9:e89004. doi:10.1371/journal.pone.0089004

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zhu Y, Shang H, Zhu Q, Ji F, Wang P, Fu J, Deng Y, Xu C, Ye W, Zheng J, Zhu L (2011) Complete genome sequence of Bacillus thuringiensis serovar finitimus strain YBT-020. J Bacteriol 193:2379–2380. doi:10.1128/JB.00267-11

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhu L, Tian LJ, Zheng J, Gao QL, Wang YY, Peng DH, Ruan LF, Sun M (2015a) Complete genome sequence of Bacillus thuringiensis serovar galleriae strain HD-29, a typical strain of commercial biopesticide. J Biotechnol 195:108–109. doi:10.1016/j.jbiotec.2014.12.021

    CAS  PubMed  Article  Google Scholar 

  • Zhu L, Peng D, Wang Y, Ye W, Zheng J, Zhao C, Han D, Geng C, Ruan L, He J, Yu Z (2015b) Genomic and transcriptomic insights into the efficient entomopathogenicity of Bacillus thuringiensis. Sci Rep 5. doi:10.1038/srep14129

  • Zhu J, Zhang Q, Cao Y, Li Q, Zhu Z, Wang L, Li P (2016) The complete genome sequence of Bacillus thuringiensis serovar Hailuosis YWC2-8. J Biotechnol 219:38–39. doi:10.1016/j.jbiotec.2015.12.016

    CAS  PubMed  Article  Google Scholar 

  • Zi-Quan Y, Qian-Lan W, Bin L, Xue Z, Zi-Niu Y, Ming S (2008) Bacillus thuringiensis crystal protein toxicity against plant-parasitic nematodes. Chinese J Agric Biotechnol 5: 13–17. doi: 10.1017/S1479236208002003

  • Zorzetti J, Ricietto AP, da Silva CR, Wolf IR, Vilas-Bôas GT, Neves PM, Meneguim AM, Vilas-Boas LA (2015) Genome sequence of the mosquitocidal Bacillus thuringiensis strain BR58, a biopesticide product effective against the coffee berry borer (Hypothenemus hampei). Genome Announc 3:e01232–e01215. doi:10.1128/genomeA.01232-15

    PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgments

The authors thank colleagues of Microbial Biotechnology Department of ABRII for their help and assistance in preparing the review paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gholamreza Salehi Jouzani.

Ethics declarations

Funding

This work was partially funded by ABRII as a part of the project with number 1-013-140000-05-8512-0000.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jouzani, G.S., Valijanian, E. & Sharafi, R. Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl Microbiol Biotechnol 101, 2691–2711 (2017). https://doi.org/10.1007/s00253-017-8175-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8175-y

Keywords

  • Anticancer
  • Antagonistic effect
  • Bacillus thuringiensis
  • Bioacaricide
  • Bioremediation
  • Nanoparticle biosynthesis
  • Plant growth-promoting rhizobacteria (PGPR)
  • Whole genome