Potential applications of Bacillus thuringiensis Berliner in agriculture, medicine and environment

Authors

  • Selvam Vignesh Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India – 641 003 https://orcid.org/0009-0000-6487-5605
  • Gothandaraman Rajadurai Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India – 641 003 https://orcid.org/0000-0003-0784-4129
  • Rajasekaran Raghu Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India – 641 003 https://orcid.org/0000-0001-8229-0993
  • Natarajan Balakrishnan Directorate of Research, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India – 641 003 https://orcid.org/0000-0003-3989-3486
  • Mannu Jayakanthan Department of Plant Molecular Biology and Bioinformatics, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India – 641 003 https://orcid.org/0000-0001-7444-9343
  • Subbarayalu Mohankumar Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, Tamil Nadu, India – 641 003 https://orcid.org/0000-0002-1581-7318

DOI:

https://doi.org/10.14719/pst.3977

Keywords:

Antimicrobial, Bacillus thuringiensis, bacteriocins, biopesticides, parasporins, PGPB

Abstract

Bacillus thuringiensis (Bt) is renowned for its insecticidal activity against a wide range of target pests. Bt formulations offer safe alternatives to chemical insecticides, effectively eliminating insects using toxins and enzymes such as chitinases and metalloproteases. This bacterium has transformed pest management through the development of genetically modified insect-resistant crops, providing targeted protection. Beyond pest control, Bt serves as an alternative to antibiotics, fertilizers, bioremediation agents and for nanomaterial synthesis. While its effectiveness in insect control contributes to sustainable farming practices, Bt further promotes plant growth as a biofertilizer and growth enhancer. Additionally, it plays various roles in medicine and environmental applications. Bacteriocins, proteins produced by Bt, exhibit high efficacy against pathogenic bacteria and demonstrate some fungicidal activity, offering potential applications in medicine and food preservation. Bt’s influence extends to environmental bioremediation, where it targets heavy metals and dyes. It is also involved in the synthesis of metal nanoparticles and exhibits anti-cancer activity by targeting various cancerous cells. Overall, Bt showcases a broad spectrum of activity across agriculture, medicine and environmental sectors, highlighting its potential to enhance crop productivity, improve human health and reduce environmental pollution.

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References

Pretty J. Agricultural sustainability: concepts, principles and evidence. Philos Trans R Soc B Biol Sci. 2008;363(1491):447-65. https://doi.org/10.1098/rstb.2007.2163

Hajek AE, Eilenberg J. Natural enemies: an introduction to biological control. 2nd ed. Cambridge University Press; 2018. https://doi.org/10.1017/9781107280267

Mnif I, Ghribi D. Potential of bacterial derived biopesticides in pest management. Crop Prot. 2015;77:52-64. https://doi.org/10.1016/j.cropro.2015.07.017

Deravel J, Lemière S, Coutte F, Krier F, Van Hese N, Béchet M, et al. Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl Microbiol Biotechnol. 2014;98:6255-64. https://doi.org/10.1007/s00253-014-5663-1

Gupta M, Kumar H, Kaur S. Vegetative insecticidal protein (Vip): potential contender from Bacillus thuringiensis for efficient management of various detrimental agricultural pests. Front Microbiol. 2021;12:659736. https://doi.org/10.3389/fmicb.2021.659736.

Santos EN, Menezes LP, Dolabellaa SS, Santini A, Severino P, Capasso R, et al. Bacillus thuringiensis: From biopesticides to anticancer agents. Biochimie. 2022;192:83-90. https://doi.org/10.1016/j.biochi.2021.10.003.

Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, et al. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev. 1998;62(3):775-806. https://doi.org/10.1128/mmbr.62.3.775-806.1998

Gothandaraman R, Venkatasamy B, Thangavel T, Eswaran K, Subbarayalu M. Molecular characterization and toxicity evaluation of indigenous Bacillus thuringiensis isolates against key lepidopteran insect pests. Egypt J Biol Pest Control. 2022;32(1):1-11. https://doi.org/10.1186/s41938-022-00639-y

Rajadurai G, Anandakumar S, Raghu R. Bacillus thuringiensis in pest management. Plant Health Archives. 2023a;1(1):11-13. https://doi.org/10.54083/PHA/1.1.2023/11-13

Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N. Bacillus thuringiensis: an impotent pathogen?. Trends Microbiol. 2010;18(5):189-94. https://doi.org/10.1016/j.tim.2010.02.006

Crickmore N, Berry C, Panneerselvam S, Mishra R, Connor TR, Bonning BC. A structure-based nomenclature for Bacillus thuringiensis and other bacteria-derived pesticidal proteins. J Invertebr Pathol. 2020;107438. https://doi.org/10.1016/j.jip.2020.107438

Lecadet MM. Bacillus thuringiensis toxins—the proteinaceous crystal. Bacterial Protein Toxins. 2013;3:437-71.

Salehi Jouzani G, Pourjan Abad A, Seifinejad A, Marzban R, Kariman K, Maleki B. 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. 2008a;35(2):83-94. https://doi.org/10.1007/s10295-007-0269-6

Alves GB, de Oliveira EE, Jumbo LOV, Dos Santos GR, Dos Santos MM, Ootani MA, et al. Genomic–proteomic analysis of a novel Bacillus thuringiensis strain: toxicity against two lepidopteran pests, abundance of Cry1Ac5 toxin and presence of INHA1 virulence factor. Arch Microbiol. 2023;205(4):143. https://doi.org/10.1007/s00203-023-03479-y

Berryish Metha C, Rajadurai G, Raghu R, Jayakanthan M, Kokiladevi E, Murugan M, Balasubramani V. Molecular characterization and nematicidal activity of indigenous Bacillus thuringiensis isolate T210. Biol Forum. 2023;15(9):274-81.

Sujayanand GK, Akram M, Konda A, Nigam A, Bhat S, Dubey J, Muthusamy SK. Distribution and toxicity of Bacillus thuringiensis (Berliner) strains from different crop rhizosphere in Indo-Gangetic plains against polyphagous lepidopteran pests. Int J Trop Insect Sci. 2021;1-19. https://doi.org/10.1007/s42690-021-00451-5

Baum JA, Johnson TB, Carlton BC. Bacillus thuringiensis. In: Hall, F.R., Menn, J.J. (eds) Biopesticides: Use and Delivery. Methods in Biotechnology, vol 5. Humana Press; 1999:189-209. https://doi.org/10.1385/0-89603-515-8:189

Burges HD, Jones KA. Formulation of bacteria, viruses and protozoa to control insects. Formulation of Microbial Biopesticides: Beneficial Microorganisms, Nematodes and Seed Treatments. 1998;33-127. https://doi.org/10.1007/978-94-011-4926-6_3

Kronstad JW, Schnepf HE, Whiteley HR. Diversity of locations for Bacillus thuringiensis crystal protein genes. J Bacteriol. 1983;154(1):419-28. https://doi.org/10.1128/jb.154.1.419-428.1983

Land M, Miljand M. Biological control of mosquitoes using Bacillus thuringiensis israelensis: a pilot study of effects on target organisms, non-target organisms and humans. Mistra EviEM, Sweden; 2014. https://doi.org/10.13140/RG.2.1.3586.5361

Marzban R, Babaei J, Kalantari M, Saberi F. Preparation of wettable powder formulation of Bacillus thuringiensis KD2. J Appl Biol Sci. 2021;15(3):285-93. https://www.jabsonline.org/index.php/jabs/article/view/830/667

Vimala Devi PS, Duraimurugan P, Chandrika KSVP, Vineela V. Development of a water dispersible granule (WDG) formulation of Bacillus thuringiensis for the management of Spodoptera litura (Fab.). Biocont Sci Technol. 2021;31(8):850-64. https://doi.org/10.1080/09583157.2021.1895073

Vijayakumar A, Mandodan SKA, Gangmei K, Padmanaban H, Bora B, Lukose J, et al. A new aqueous formulation from indigenously isolated Bacillus thuringiensis israelensis VCRC B646 for mosquito control. Indian J Entomol. 2024;e24876. https://doi.org/10.55446/IJE.2024.1876

Chang WT, Chen ML, Wang SL. An antifungal chitinase produced by Bacillus subtilis using chitin waste as a carbon source. World J Microbiol Biotechnol. 2010;26:945-50. https://doi.org/10.1007/s11274-009-0244-7

Rathore AS, Gupta RD. Chitinases from bacteria to human: properties, applications and future perspectives. Enzyme Res. 2015;791907. https://doi.org/10.1155/2015/791907

Agrawal S, Kelkenberg M, Begum K, Steinfeld L, Williams CE, Kramer KJ, et al. Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem Mol Biol. 2014;49:24-34. https://doi.org/10.1016/j.ibmb.2014.03.009

Dalhammar G, Steiner H. Characterization of inhibitor A, a protease from Bacillus thuringiensis which degrades attacins and cecropins, two classes of antibacterial proteins in insects. Eur J Biochem. 1984;139(2):247-52. https://doi.org/10.1111/j.1432-1033.1984.tb08000.x

Wan L, Lin J, Du H, Zhang Y, Bravo A, Soberón M, et al. Bacillus thuringiensis targets the host intestinal epithelial junctions for successful infection of Caenorhabditis elegans. Environ Microbiol. 2019;21(3):1086-98. https://doi.org/10.1111/1462-2920.14528

Fricke B, Drößler K, Willhardt I, Schierhorn A, Menge S, Rücknagel P. The cell envelope-bound metalloprotease (camelysin) from Bacillus cereus is a possible pathogenic factor. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 2001;1537(2):132-46. https://doi.org/10.1016/S0925-4439(01)00066-7

Nishiwaki H, Nakashima K, Ishida C, Kawamura T, Matsuda K. Cloning, functional characterization and mode of action of a novel insecticidal pore-forming toxin, sphaericolysin, produced by Bacillus sphaericus. Appl Environ Microbiol. 2007;73(10):3404-11. https://doi.org/10.1128/AEM.00021-07

Zhang X, Liang Z, Siddiqui ZA, Gong Y, Yu Z, Chen S. Efficient screening and breeding of Bacillus thuringiensis subsp. kurstaki for high toxicity against Spodoptera exigua and Heliothis armigera. J Ind Microbiol Biotechnol. 2009;36(6):815-20. https://doi.org/10.1007/s10295-009-0556-5

Iatsenko I, Nikolov A, Sommer RJ. Identification of distinct Bacillus thuringiensis 4A4 nematicidal factors using the model nematodes Pristionchus pacificus and Caenorhabditis elegans. Toxins. 2014;6(7):2050-63. https://doi.org/10.3390/toxins6072050

Royalty RN, Hall FR, Taylor RAJ. Effects of thuringiensin on Tetranychus urticae (Acari: Tetranychidae) mortality, fecundity and feeding. J Econ Entomol. 1990;83(3):792-98. https://doi.org/10.1093/jee/83.3.792

Tsai SF, Yang C, Liu BL, Hwang JS, Ho SP. Role of oxidative stress in thuringiensin-induced pulmonary toxicity. Toxicol Appl Pharmacol. 2006;216(2):347-53. https://doi.org/10.1016/j.taap.2006.05.013

Zheng J, Gao Q, Liu L, Liu H, Wang Y, Peng D, et al. Comparative genomics of Bacillus thuringiensis reveals a path to specialized exploitation of multiple invertebrate hosts. mBio. 2017;8(4):e00822-17. https://doi.org/10.1128/mBio.00822-17

Jouzani GS, Valijanian E, Sharafi R. Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. BioSafety. 2017; 101:2691-711. https://doi.org/10.1007/s00253-017-8175-y

Muddanuru T, Polumetla AK, Maddukuri L, Mulpuri S. Development and evaluation of transgenic castor (Ricinus communis L.) expressing the insecticidal protein Cry1Aa of Bacillus thuringiensis against lepidopteran insect pests. Crop Prot. 2019;119:113-25. https://doi.org/10.1016/j.cropro.2019.01.016

Rajadurai G, Kalaivani A, Varanavasiyappan S, Balakrishnan N, Udayasuriyan V, Sudhakar D, Natarajan N. Generation of insect resistant marker-free transgenic rice with a novel cry2AX1 gene. Electron J Plant Breed. 2018;9(2):723-32. https://doi.org/10.5958/0975-928X.2018.00086.8

Rajadurai G, Sudhakar D, Varanavasiappan S, Balakrishnan N, Udayasuriyan V, Natarajan N. Adult oviposition preference and larval performance of Cnaphalocrocis medinalis Guenee (Pyralidae: Lepidoptera) on transgenic Bt rice. Int J Trop Insect Sci. 2023;43(3):1037-48. https://doi.org/10.1007/s42690-023-01026-2

Sadek HE, Ebadah IM, Mahmoud YA. Importance of biotechnology in controlling insect pests. J Mod Agric Biotechnol. 2023;2(1):5. https://www.doi.org/10.53964/jmab.2023005

ISAAA. Global status of commercialized biotech. GM Crops in 2019 (ISAAA Brief 55). Available at https://www.isaaa.org/resources/publications/briefs/55/default.asp (Accessed on February 20, 2024).

ISAAA. ISAAA’s GM Approval Database. 2024. Available at https://www.isaaa.org/gmapprovaldatabase/ (Accessed on January 31, 2024).

Abbas MST. Genetically engineered (modified) crops (Bacillus thuringiensis crops) and the world controversy on their safety. Egypt J Biol Pest Control. 2018;28(1):1-12. https://doi.org/10.1186/s41938-018-0051-2

Mendelshon M, Kough J, Vaituzis Z, Mathews K. Are Bt crops safe? Nat Biotechnol. 2003;21(9):1003-09. https://doi.org/10.1038/nbt0903-1003

Lu YH. Mirid bug outbreaks in multiple crops correlated with wide scale adoption of Bt cotton in China. Science. 2010;328:1151-54. https://doi.org/10.1126/science.1187881

Losey JE, Rayor LS, Carter ME. Transgenic pollen harms monarch larvae. Nature. 1999;399:214. https://doi.org/10.1038/20338

Moussa S, Baiomy F, Abouzaid K, Nasr M, Moussa EA, Kamel EA. Potential impact of host pest fed on Bt corn on the development of Chrysoperla carnea (Neur.: Chrysopidae). Egypt J Biol Pest Control. 2018;28(23):1-6. https://doi.org/10.1186/s41938-017-0018-8

Duan JJ, Marvier M, Huesing J, Dively G, Huang ZY. A meta-analysis of effects of Bt toxins on honeybees. PLoS One. 2008;3(1):e1415. https://doi.org/10.1371/journal.pone.0001415

Doshi MN, Badr K, Ejaz M, Hassan ZU, Jaoua S. Investigation of novel bacteriocin producers of Bacillus thuringiensis and partial characterization of two new bacteriocins: Thuricin 466 and thuricin 4Q7. Bioresour Technol Rep. 2024; 25:101760. https://doi.org/10.1016/j.biteb.2024.101760

Liu Z, Pang H, Yi K, Wang X, Zhang W, Zhang C, et al. Isolation and application of Bacillus thuringiensis LZX01: Efficient membrane biofouling mitigation function and anti-toxicity potential. Bioresour Technol. 2024;130272. https://doi.org/10.1016/j.biortech.2023.130272

Peng Z, Wang D, He Y, Wei Z, Xie M, Xiong T. Gut distribution, impact factor and action mechanism of bacteriocin-producing beneficial microbes as promising antimicrobial agents in gastrointestinal infection. Probiotics Antimicrob Proteins. 2024;1-12. https://doi.org/10.1007/s12602-024-10222-6

Bora LC, Kataki L, Talukdar K, Nath BC, Sarkar R. 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 Agric Sci. 2015;3(2). https://doi.org/10.18006/jebas.030201

Jeong H, Jo SH, Hong CE, Park JM. Genome sequence of the endophytic bacterium Bacillus thuringiensis strain KB1, a potential biocontrol agent against phytopathogens. Genome Announc. 2016;4(2):10-1128. https://doi.org/10.1128/genomea.00279-16

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

Y?lmaz S, Idris AB, Ayvaz A, Temizgül R, Hassan MA. Whole-genome sequencing of Bacillus thuringiensis strain SY49. 1 reveals the detection of novel candidate pesticidal and bioactive compounds isolated from Turkey. bioRxiv. 2022;03. https://doi.org/10.1101/2022.03.07.482483

Barboza-Corona JE, Vázquez-Acosta H, Bideshi DK, Salcedo-Hernández R. Bacteriocin-like inhibitor substances produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol. 2007;187:117-26. https://doi.org/10.1007/s00203-006-0178-5

de la Fuente-Salcido NM, Casados-Vázquez LE, Barboza-Corona JE. Bacteriocins of Bacillus thuringiensis can expand the potential of this bacterium to other areas rather than limit its use only as microbial insecticide. Can J Microbiol. 2013;59(8):515-22. https://doi.org/10.1139/cjm-2013-0284

Oktarina H, Husna A, Nafida JT, Pramayudi N, Chamzurni T. A study on the potential of Bacillus thuringiensis AK08 to control pathogenic fungi associated with chili plant. In: IOP Conference Series: Earth and Environmental Science, IOP Publishing; 2024. 1297(1): 012073. https://doi.org/10.1088/1755-1315/1297/1/012073

Wang M, Geng L, Jiao S, Wang K, Xu W, Shu C, Zhang J. Bacillus thuringiensis exopolysaccharides induced systemic resistance against Sclerotinia sclerotiorum in Brassica campestris L. Biol Control. 2023;183:105267. https://doi.org/10.1016/j.biocontrol.2023.105267

Abdeljalil NOB, Vallance J, Gerbore J, Yacoub A, Daami-Remadi M, Rey P. Combining potential oomycete and bacterial biocontrol agents as a tool to fight tomato Rhizoctonia root rot. Biol Control. 2021;155:104521. https://doi.org/10.1016/j.biocontrol.2020.104521

Martínez-Absalón S, Rojas-Solís D, Hernández-León R, Prieto-Barajas C, Orozco-Mosqueda MDC, Peña-Cabriales JJ, et al. 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 Technol. 2014;24(12):1349-62. https://doi.org/10.1080/09583157.2014.940846

Roy A, Mahata D, Paul D, Korpole S, Franco OL, Mandal SM. Purification, biochemical characterization and self-assembled structure of a fengycin-like antifungal peptide from Bacillus thuringiensis strain SM1. Front Microbiol. 2013;4:332. https://doi.org/10.3389/fmicb.2013.00332

Fatima R, Mahmood T, Moosa A, Aslam MN, Shakeel MT, Maqsood A, et al. Bacillus thuringiensis CHGP12 uses a multifaceted approach for the suppression of Fusarium oxysporum f. sp. ciceris and to enhance the biomass of chickpea plants. Pest Manag Sci. 2023;79(1):336-48. https://doi.org/10.1002/ps.7203

Azizoglu U. Bacillus thuringiensis as a biofertilizer and biostimulator: A mini-review of the little-known plant growth-promoting properties of Bt. Curr Microbiol. 2019;76(11):1379-85. https://doi.org/10.1007/s00284-019-01705-9

Delfim J, Dijoo ZK. Bacillus thuringiensis as a biofertilizer and plant growth promoter. In: G. H. Dar, R. A. Bhat, M. A. Mehmood and K. R. Hakeem (Eds.). Microbiota and Biofertiliz ers: Ecofriendly Tools for Reclamation of Degraded Soil Environs. Springer International Publishing; 2021.2:251-65. https://doi.org/10.1007/978-3-030-61010-4_12

Azizoglu U, Salehi Jouzani G, Sansinenea E, Sanchis-Borja V. Biotechnological advances in Bacillus thuringiensis and its toxins: Recent updates. Reviews in Environmental Science and Bio/technology. 2023;22(2):319-48. https://doi.org/10.1007/s11157-023-09652-5

Öztopuz O, Pekin G, Park RD, Eltem R. Isolation and evaluation of new antagonist Bacillus strains for the control of pathogenic and mycotoxigenic fungi of fig orchards. Appl Biochem Biotechnol. 2018;186(3):692-711. https://doi.org/10.1007/s12010-018-2764-9

Djenane Z, Nateche F, Amziane M, Gomis-Cebolla J, El-Aichar F, Khorf H, Ferré J. Assessment of the antimicrobial activity and the entomocidal potential of Bacillus thuringiensis isolates from Algeria. Toxins. 2017;9(4):139. https://doi.org/10.3390/toxins9040139

Hernández-Huerta J, Tamez-Guerra P, Gomez-Flores R, Delgado Gardea MCE, Robles-Hernández L, Gonzalez-Franco AC, Infante-Ramirez R. Pepper growth promotion and bio control against Xanthomonas euvesicatoria by Bacillus cereus and Bacillus thuringiensis formulations. PeerJ. 2023;11:e14633. https://doi.org/10.7717/peerj.14633

Yoshida S, Koitabashi M, Yaginuma D, Anzai M, Fukuda M. Potential of bioinsecticidal Bacillus thuringiensis inoculum to suppress gray mold in tomato based on induced systemic resistance. J Phytopathol. 2019;167(11-12):679-85. https://doi.org/10.1111/jph.12864

Gupta R, Keppanan R, Leibman-Markus M, Matveev S, Rav-David D, Shulhani R, Bar M. Bacillus thuringiensis promotes systemic immunity in tomato, controlling pests and pathogens and promoting yield. Food Sec. 2024;1-16. https://doi.org/10.1007/s12571-024-01441-4

Zhang F, Dashti N, Hynes RK, Smith DL. Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann Bot. 1996;77(5):453-60. https://doi.org/10.1006/anbo.1996.0055

Zhang F, Dashti N, Hynes RK, Smith DL. Plant growth-promoting rhizobacteria and soybean [Glycine max (L.) Merr.] growth and physiology at suboptimal root zone temperatures. Ann Bot. 1997;79(3):243-49. https://doi.org/10.1006/anbo.1996.0332

Vidal-Quist JC, Rogers HJ, Mahenthiralingam E, Berry C. Bacillus thuringiensis colonises plant roots in a phylogeny-dependent manner. FEMS Microbiol Ecol. 2013;86(3):474-89. https://doi.org/10.1111/1574-6941.12175

Qi J, Aiuchi D, Tani M, Asano SI, Koike M. Potential of entomopathogenic Bacillus thuringiensis as plant growth promoting rhizobacteria and biological control agents for tomato Fusarium wilt. Int J Environ Agric Res. 2016;2(6):55-63.

Pindi PK, Sultana T, Vootla PK. Plant growth regulation of Bt-cotton through Bacillus species. 3 Biotech. 2014;4:305-15. https://doi.org/10.1007/s13205-013-0154-0

Gomes A, Mariano RL, Silveira EB, Mesquita JC. Isolation, selection of bacteria and effect of Bacillus spp. in the production of organic lettuce seedlings. Hortic Bras. 2003;21:699-703. https://doi.org/10.1590/S0102-05362003000400026

Mishra PK, Mishra S, Selvakumar G, Bisht JK, Kundu S, Gupta HS. 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. 2009;25:753-61. https://doi.org/10.1007/s11274-009-9963-z

Sharma N, Saharan B. Bacterization effect of culture containing 1-aminocyclopropane-1-carboxylic acid deaminase activity implicated for plant development. Br Microbiol Res J. 2016;16(1):1-10. https://doi.org/10.9734/BMRJ/2016/27135

Ha-Tran DM, Nguyen TTM, Hung SH, Huang E, Huang CC. Roles of plant growth-promoting rhizobacteria (PGPR) in stimulating salinity stress defense in plants: A review. Int J Mol Sci. 2021;22(6):1-38. https://doi.org/10.3390/ijms22063154

Ali B, Hafeez A, Ahmad S, Javed MA, Afridi MS, Dawoud TM, et al. Bacillus thuringiensis PM25 ameliorates oxidative damage of salinity stress in maize via regulating growth, leaf pigments, antioxidant defense system and stress responsive gene expression. Front Plant Sci. 2022;13:921668. https://doi.org/10.3389/fpls.2022.921668

Fitriatin BN, Yuniarti A, Turmuktini T, Ruswandi FK. The effect of phosphate solubilizing microbe producing growth regulators on soil phosphate, growth and yield of maize and fertilizer efficiency on Ultisol. Eurasian J Soil Sci. 2014;3(2):101-07. https://doi.org/10.18393/ejss.34313

Raddadi N, Cherif A, Ouzari H, Marzorati M, Brusetti L, Boudabous A, Daffonchio D. Bacillus thuringiensis beyond insect biocontrol: plant growth promotion and biosafety of polyvalent strains. Ann Microbiol. 2007;57:481-94. https://doi.org/10.1007/BF03175344

Wilson MK, Abergel RJ, Raymond KN, Arceneaux JE, Byers BR. Siderophores of Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis. Biochem Biophys Res Commun. 2006;348(1):320-25. https://doi.org/10.1016/j.bbrc.2006.07.055

Okafor F, Janen A, Kukhtareva T, Edwards V, Curley M. Green synthesis of silver nanoparticles, their characterization, application and antibacterial activity. Int J Environ Res Public Health. 2013;10(10):5221-38. https://doi.org/10.3390/ijerph10105221

Das VL, Thomas R, Varghese RT, Soniya EV, Mathew J, Radhakrishnan EK. Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech. 2014;4:121-26. https://doi.org/10.1007/s13205-013-0130-8

Nayak PS, Arakha M, Kumar A, Asthana S, Mallick BC, Jha S. An approach towards continuous production of silver nanoparticles using Bacillus thuringiensis. RSC Adv. 2016;6(10):8232-42. https://doi.org/10.1039/C5RA21281B

Marimuthu S, Rahuman AA, Kirthi AV, Santhoshkumar T, Jayaseelan C, Rajakumar G. Eco-friendly microbial route to synthesize cobalt nanoparticles using Bacillus thuringiensis against malaria and dengue vectors. Parasitol Res. 2013;112:4105-12. https://doi.org/10.1007/s00436-013-3601-2

Salgado P, Bustamante L, Carmona DJ, Melendrez MF, Rubilar O, Salazar C, et al. Green synthesis of Ag/Ag2O nanoparticles on cellulose paper and cotton fabric using Eucalyptus globulus leaf extracts: Toward the clarification of formation mechanism. Surf Interfaces. 2023;40:102928. https://doi.org/10.1016/j.surfin.2023.102928

Ge J, Hu J, Cui S, Wang Y, Xu C, Liu W. Biosynthesis of Bt-Ag2O nanoparticles using Bacillus thuringiensis and their pesticidal and antimicrobial activities. Appl Microbiol Biotechnol. 2024;108(1):157. https://doi.org/10.1007/s00253-023-12859-9

Karunagaran V, Rajendran K, Sen S. Optimization of biosynthesis of silver oxide nanoparticles and its anticancer activity. Int J Nanosci. 2017;16(5-6):1750018. https://doi.org/10.1142/s0219581x17500181

Agarwal H, Kumar SV, Rajeshkumar S. A review on green synthesis of zinc oxide nanoparticles – an eco-friendly approach. Resour-Effic Technol. 2017;3(4):406-13. https://doi.org/10.1016/j.reffit.2017.03.002

Jalali E, Bel Y, Maghsoudi S, Noroozian E, Escriche B. Enhancing insecticidal efficacy of Bacillus thuringiensis Cry1Ab through pH-sensitive encapsulation. Appl Microbiol Biotechnol. 2023;107(20):6407-19. https://doi.org/10.1007/s00253-023-12723-w

Jansen E, Michels M, Van Til M, Doelman P. Effects of heavy metals in soil on microbial diversity and activity as shown by the sensitivity-resistance index, an ecologically relevant parameter. Biol Fertil Soils. 1994;17:177-84. https://doi.org/10.1007/BF00336319

Hussein H, Farag S, Moawad H. Isolation and characterization of Pseudomonas resistant to heavy metals contaminants. Arab J Biotechnol. 2003;7:13-22. https://doi.org/10.2225/vol7-issue1-fulltext-2

Verma S, Kuila A. Bioremediation of heavy metals by microbial process. Environ Technol Innov. 2019;14:100369. https://doi.org/10.1016/j.eti.2019.100369

Coblenz A, Wolf K. The role of glutathione biosynthesis in heavy metal resistance in the fission yeast Schizosaccharomyces pombe. FEMS Microbiol Rev. 1994;14(4):303-08. https://doi.org/10.1111/j.1574-6976.1994.tb00103.x

Aktar N, Karim M, Khan S, Begum A. In silico studies of parasporin proteins: Structural and functional insights and proposed cancer cell killing mechanism for parasporin 5 and 6. Microbial Bioactives. 2019;2(1):82-90. https://doi.org/10.25163/microbbioacts.21007A0621280219

Mizuki E, Ohba M, Akao T, Yamashita S, Saitoh H, Park YS. Unique activity associated with non-insecticidal Bacillus thuringiensis parasporal inclusions: in vitro cell-killing action on human cancer cells. J Appl Microbiol. 1999;86(3):477-86. https://doi.org/10.1046/j.1365-2672.1999.00692.x

Mizuki E, Park YS, Saitoh H, Yamashita S, Akao T, Higuchi K, Ohba M. Parasporin, a human leukemic cell-recognizing parasporal protein of Bacillus thuringiensis. Clin Diagn Lab Immunol. 2000;7(4):625-34. https://doi.org/10.1128/cdli.7.4.625-634.2000

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

Ohba M, Mizuki E, Uemori A. Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Res. 2009;29(1):427-33. https://pubmed.ncbi.nlm.nih.gov/19331182/

Akiba T, Okumura S. Parasporins 1 and 2: their structure and activity. J Invertebr Pathol. 2017;142:44-49. https://doi.org/10.1016/j.jip.2016.10.005

Lenina NK, Naveenkumar A, Sozhavendan AE, Balakrishnan N, Balasubramani V, Udayasuriyan V. Characterization of parasporin gene harboring Indian isolates of Bacillus thuringiensis. 3 Biotech. 2014;4:545-51. https://doi.org/10.1007/s13205-013-0190-9

Nagamatsu Y, Okamura S, Saitou H, Akao T, Mizuki E. Three Cry toxins in two types from Bacillus thuringiensis strain M019 preferentially kill human hepatocyte cancer and uterus cervix cancer cells. Biosci Biotechnol Biochem. 2010;74(3):494-98. https://doi.org/10.1271/bbb.90615

Ekino K, Okumura S, Ishikawa T, Kitada S, Saitoh H, Akao T, et al. Cloning and characterization of a unique cytotoxic protein parasporin-5 produced by Bacillus thuringiensis A1100 strain. Toxins. 2014;6(6):1882-95. https://doi.org/10.3390/toxins6061882

Xu C, Wang BC, Yu Z, Sun M. Structural insights into Bacillus thuringiensis Cry, Cyt and parasporin toxins. Toxins. 2014;6(9):2732-70. https://doi.org/10.3390/toxins6092732

Katayama H, Kusaka Y, Yokota H, Akao T, Kojima M, Nakamura O, et al. Parasporin-1, a novel cytotoxic protein from Bacillus thuringiensis, induces Ca2+ influx and a sustained elevation of the cytoplasmic Ca2+ concentration in toxin-sensitive cells. J Biol Chem. 2007;282(10):7742-52. https://doi.org/10.1074/jbc.M611382200

Shimada H, Kitada S. Mega assemblages of oligomeric aerolysin-like toxins stabilized by toxin-associating membrane proteins. Int J Biochem. 2011;149(1):103-15. https://doi.org/10.1093/jb/mvq124

Abe Y, Inoue H, Ashida H, Maeda Y, Kinoshita T, Kitada S. Glycan region of GPI anchored-protein is required for cytocidal oligomerization of an anticancer parasporin-2, Cry46Aa1 protein, from Bacillus thuringiensis strain A1547. J Invertebr Pathol. 2017;142:71-81. https://doi.org/10.1016/j.jip.2016.11.008

Krishnan V, Domanska B, Elhigazi A, Afolabi F, West MJ, Crickmore N. The human cancer cell active toxin Cry41Aa from Bacillus thuringiensis acts like its insecticidal counterparts. Biochem J. 2017;474(10):1591-602. https://doi.org/10.1042/BCJ20170122

Okumura S, Akao T, Higuchi K, Saitoh H, Mizuki E, Ohba M, Inouye K. Bacillus thuringiensis serovar shandongiensis strain 89-T-34-22 produces multiple cytotoxic proteins with similar molecular masses against human cancer cells. Lett Appl Microbiol. 2004;39(1):89-92. https://doi.org/10.1111/j.1472-765X.2004.01544.x

Okassov A, Nersesyan A, Kitada S, Ilin A. Parasporins as new natural anticancer agents: a review. J Buon. 2015;20(1):5. https://pubmed.ncbi.nlm.nih.gov/25778289/

Suárez-Barrera MO, Visser L, Rondón-Villarreal P, Herrera-Pineda DF, Alarcón-Aldana JS, Van den Berg A, et al. Genetic modification approaches for parasporins Bacillus thuringiensis proteins with anticancer activity. Mol. 2021;26(24):7476. https://doi.org/10.3390/molecules26247476

Jain D, Kachhwaha S, Jain R, Srivastava G, Kothari SL. Novel microbial route to synthesize silver nanoparticles using spore crystal mixture of Bacillus thuringiensis. Indian J Exp Biol. 2010;48(11):1152-56. http://nopr.niscpr.res.in/handle/123456789/10471

Najitha Banu A, Balasubramanian C, Moorthi PV. Biosynthesis of silver nanoparticles using Bacillus thuringiensis against dengue vector, Aedes aegypti (Diptera: Culicidae). Parasitol Res. 2014;113:311-16. https://doi.org/10.1007/s00436-013-3656-0

Afolayan EM, Afegbua SL, Ado SA. Characterization and antibacterial activity of silver nanoparticles synthesized by soil-dwelling Bacillus thuringiensis against drug-resistant bacteria. Biol. 2023;1-10. https://doi.org/10.1007/s11756-023-01381-y

Hassen A, Saidi N, Cherif M, Boudabous A. Effects of heavy metals on Pseudomonas aeruginosa and Bacillus thuringiensis. Bioresour Technol. 1998;65(1-2):73-82. https://doi.org/10.1016/S0960-8524(98)00011-X

Kumar P, Chandra R. Detoxification of distillery effluent through Bacillus thuringiensis (MTCC 4714) enhanced phytoremediation potential of Spirodela polyrrhiza (L.) Schliden. Bull Environ Contam Toxicol. 2004;73:903-10. https://doi.org/10.1007/s00128-004-0512-z

Kumar P, Chandra R. Decolourisation and detoxification of synthetic molasses melanoidins by individual and mixed cultures of Bacillus spp. Bioresour Technol. 2006;97(16):2096-102. https://doi.org/10.1016/j.biortech.2005.10.012

El-Sersy NA. Bioremediation of methylene blue by Bacillus thuringiensis 4 G 1: application of statistical designs and surface plots for optimization. J Biotech. 2007;6(1):34-39. https://doi.org/10.3923/biotech.2007.34.39

Zeinat Kamal M, Nashwa AH, Mohamed AI, Sherif EN. Biodegradation and detoxification of malathion by of Bacillus thuringiensis MOS-5. Aust J Basic Appl Sci. 2008;2(3):724-32.

Poopathi S, Abidha S. Biodegradation of poultry waste for the production of mosquitocidal toxins. Int Biodeterior Biodegradation. 2008;62(4):479-82. https://doi.org/10.1016/j.ibiod.2008.03.005

Brar SK, Verma M, Tyagi RD, Valéro JR, Surampalli RY. Concurrent degradation of dimethyl phthalate (DMP) during production of Bacillus thuringiensis based biopesticides. J Hazard Mater. 2009;171(1-3):1016-23. https://doi.org/10.1016/j.jhazmat.2009.06.108

Dave SR, Dave RH. Isolation and characterization of Bacillus thuringiensis for Acid red 119 dye decolourisation. Bioresour Technol. 2009;100(1):249-53. https://doi.org/10.1016/j.biortech.2008.05.019

Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, et al. Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Bioresour Technol. 2010;101(22):8599-605. https://doi.org/10.1016/j.biortech.2010.06.085

Maiti A, Das S, Bhattacharyya N. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons by Bacillus thuringiensis strain NA2. J Sci. 2012;1(4):72-75.

Mandal K, Singh B, Jariyal M, Gupta VK. Microbial degradation of fipronil by Bacillus thuringiensis. Ecotoxicol Environ Saf. 2013;93:87-92. https://doi.org/10.1016/j.ecoenv.2013.04.001

Thamer M, Al-Kubaisi AR, Zahraw Z, Abdullah HA, Hindy I, Abd Khadium A. Biodegradation of Kirkuk light crude oil by Bacillus thuringiensis, Northern of Iraq. J Nat Sci. 2013;5(7):34122. https://doi.org/10.4236/ns.2013.57104

Olukanni OD, Adenopo A, Awotula AO, Osuntoki AA. Biodegradation of malachite green by extracellular laccase producing Bacillus thuringiensis RUN1. J Basic Appl Sci. 2013;9:543. https://doi.org/10.6000/1927-5129.2013.09.70

Sukhumungoon P, Rattanachuay P, Hayeebilan F, Kantachote D. Biodegradation of ethidium bromide by Bacillus thuringiensis isolated from soil. Afr J Microbiol Res. 2013;7(6):471-76. https://doi.org/10.5897/AJMR12.1642

Oves M, Khan MS, Zaidi A. Biosorption of heavy metals by Bacillus thuringiensis strain OSM29 originating from industrial effluent contaminated north Indian soil. Saudi J Biol Sci. 2013;20(2):121-29. https://doi.org/10.1016/j.sjbs.2012.11.006

Babu AG, Kim JD, Oh BT. Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J Hazard Mater. 2013;250:477-83. https://doi.org/10.1016/j.jhazmat.2013.02.014

Surhio MA, Talpur FN, Nizamani SM, Amin F, Bong CW, Lee CW, et al. Complete degradation of dimethyl phthalate by biochemical cooperation of the Bacillus thuringiensis strain isolated from cotton field soil. RSC Adv. 2014;4(99):55960-66. https://doi.org/10.1039/C4RA09465D

Dash HR, Mangwani N, Das S. Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Pollut Res. 2014;21:2642-53. https://doi.org/10.1007/s11356-013-2206-8

Das P, Sinha S, Mukherjee SK. Nickel bioremediation potential of Bacillus thuringiensis KUNi1 and some environmental factors in nickel removal. Biorem J. 2014;18(2):169-77.

https://doi.org/10.1080/10889868.2014.889071

Huang TP, Ying X, Jie-Ru PAN, Zhi C, Li-Fen LI, Lei XU, et al. Aerobic Cr (VI) reduction by an indigenous soil isolate Bacillus thuringiensis BRC-ZYR2. Pedosphere. 2014;24(5):652-61. https://doi.org/10.1016/S1002-0160(14)60051-5

Pan X, Chen Z, Chen F, Cheng Y, Lin Z, Guan X. The mechanism of uranium transformation from U (VI) into nano-uramphite by two indigenous Bacillus thuringiensis strains. J Hazard Mater. 2015;297:313-19. https://doi.org/10.1016/j.jhazmat.2015.05.019

Chen Z, Pan X, Chen H, Lin Z, Guan X. Investigation of lead (II) uptake by Bacillus thuringiensis 016. World J Microbiol Biotechnol. 2015;31:1729-36. https://doi.org/10.1007/s11274-015-1923-1

Aceves-Diez AE, Estrada-Castañeda KJ, Castañeda-Sandoval LM. Use of Bacillus thuringiensis supernatant from a fermentation process to improve bioremediation of chlorpyrifos in contaminated soils. J Environ Manag. 2015;157:213-19. https://doi.org/10.1016/j.jenvman.2015.04.026

Chen S, Deng Y, Chang C, Lee J, Cheng Y, Cui Z, et al. Pathway and kinetics of cyhalothrin biodegradation by Bacillus thuringiensis strain ZS-19. Sci Rep. 2015;5(1):8784. https://doi.org/10.1038/srep08784

Wu S, Peng Y, Huang Z, Huang Z, Xu L, Ivan G, et al. Isolation and characterization of a novel native Bacillus thuringiensis strain BRC-HZM2 capable of degrading chlorpyrifos. J Basic Microbiol. 2015;55(3):389-97. https://doi.org/10.1002/jobm.201300501

Kumar V, Singh S, Kashyap N, Singla S, Bhadrecha P, Kaur P, et al. Bioremediation of heavy metals by employing resistant microbial isolates from agricultural soil irrigated with industrial waste water. Orient J Chem. 2015;31(1):357-61. http://dx.doi.org/10.13005/ojc/310142

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

Jahan N, Idrees M, Zahid M, Ali N, Hussain M. Molecular identification and characterization of heavy metal resistant bacteria and their role in bioremediation of chromium. Br Microbiol Res J. 2016;13(6):1-11. https://doi.org/10.9734/BMRJ/2016/22909

Marchlewicz A, Domaradzka D, Guzik U, Wojcieszy?ska D. Bacillus thuringiensis B1 (2015b) is a Gram-positive bacteria able to degrade naproxen and ibuprofen. Wat Air and Soil Poll. 2015;227:1-8. https://doi.org/10.1007/s11270-016-2893-0

Surhio MA, Talpu FN, Nizamani SM, Talpur MK, Amin F, Khaskheli AA, et al. Effective bioremediation of endocrine-disrupting phthalate esters, mediated by Bacillus strains. Wat Air and Soil Poll. 2017; 228:1-8. https://doi.org/10.1007/s11270-017-3567-2

Ereqat SI, Abdelkader AA, Nasereddin AF, Al-Jawabreh AO, Zaid TM, Letnik I, Abdeen ZA. Isolation and characterization of phenol degrading bacterium strain Bacillus thuringiensis J20 from olive waste in Palestine. J Environ Sci Heal A. 2018;53(1):39-45. https://doi.org/10.1080/10934529.2017.1368300

Bhatt P, Huang Y, Zhang W, Sharma A, Chen S. Enhanced cypermethrin degradation kinetics and metabolic pathway in Bacillus thuringiensis strain SG4. Microorganisms. 2020;8(2):223. https://doi.org/10.3390/microorganisms8020223

Oyewusi HA, Wahab RA, Kaya Y, Edbeib MF, Huyop F. Alternative bioremediation agents against haloacids, haloacetates and chlorpyrifos using novel halogen-degrading bacterial isolates from the hypersaline lake Tuz. Catalysts. 2020;10(6):651. https://doi.org/10.3390/catal10060651

Hsieh HY, Lin CH, Hsu SY, Stewart GC. A Bacillus spore-based display system for bioremediation of atrazine. Appl Environ Microbiol. 2020;86(18):e01230-20. https://doi.org/10.1128/AEM.01230-20

Kara AK, Fak?o?lu Ö, Kotan R, Atamanalp M, Alak G. The investigation of bioremediation potential of Bacillus subtilis and B. thuringiensis isolates under controlled conditions in freshwater. Arch Microbiol. 2021;203:2075-85. https://doi.org/10.1007/s00203-021-02187-9

Darwesh OM, Mahmoud MS, Barakat KM, Abuellil A, Ahmad MS. Improving the bioremediation technology of contaminated wastewater using biosurfactants produced by novel bacillus isolates. Heliyon. 2021;7(12). https://doi.org/10.1016/j.heliyon.2021.e08616

Suresh G, Balasubramanian B, Ravichandran N, Ramesh B, Kamyab H, Velmurugan PP, et al. Bioremediation of hexavalent chromium-contaminated wastewater by Bacillus thuringiensis and Staphylococcus capitis isolated from tannery sediment. Biomass Convers Biorefin. 2021;11:383-91. https://doi.org/10.1007/s13399-020-01259-y

Hsu SY, Hsieh HY, Stewart GC, Lin CH. Bioremediation of atrazine and its metabolite using multiple enzymes delivered by a Bacillus thuringiensis spore display system. bioRxiv. 2023;10. https://doi.org/10.1101/2023.10.31.565005

Yun SD, Lee CO, Kim HW, An SJ, Kim S, Seo MJ, et al. Exploring a new biocatalyst from Bacillus thuringiensis JNU01 for polyethylene biodegradation. Environ Technol Lett. 2023;10(6):485-92. https://doi.org/10.1021/acs.estlett.3c00189

Anbuganesan V, Vishnupradeep R, Mehnaz N, Kumar A, Freitas H, Rajkumar M. Synergistic effect of biochar and plant growth promoting bacteria improve the growth and phytostabilization potential of Sorghum bicolor in Cd and Zn contaminated soils. Rhizosphere. 2024;29:100844. https://doi.org/10.1016/j.rhisph.2023.100844.

Shahzad A, Hameed S, Qin M, Li H, Zafar S, Siddiqui S, et al. Cadmium (Cd) detoxification and plant defense enzymes activation in wheat (Triticum aestivum) by using endophytic Bacillus thuringiensis and Salix alba root powder. SSRN [preprint]. Available from: https://ssrn.com/abstract=4696234

Chen S, Gong J, Cheng Y, Guo Y, Li F, Lan T, et al. The biochemical behavior and mechanism of uranium (VI) bioreduction induced by natural Bacillus thuringiensis. J Environ Sci. 2024;136:372-81. https://doi.org/10.1016/j.jes.2022.12.001

Jung YC, Mizuki E, Akao T, Cote JC. Isolation and characterization of a novel Bacillus thuringiensis strain expressing a novel crystal protein with cytocidal activity against human cancer cells. J Appl Microbiol. 2007;103(1):65-79. https://doi.org/10.1111/j.1365-2672.2006.03260.x

Uemori A, Ohgushi A, Yasutake K, Maeda M, Mizuki E, Ohba M. Parasporin-1Ab, a novel Bacillus thuringiensis cytotoxin preferentially active on human cancer cells in vitro. Anticancer Res. 2008;28(1A):91-95. https://pubmed.ncbi.nlm.nih.gov/18383829/

Yasutake K, Uemori A, Binh ND, Mizuki E, Ohba M. Identification of parasporin genes in Vietnamese isolates of Bacillus thuringiensis. Zeitschrift für Naturforschung C. 2008;63(1-2):139-43. https://doi.org/10.1515/znc-2008-1-225

Kuroda S, Begum A, Saga M, Hirao A, Mizuki E, Sakai H, Hayakawa T. Parasporin 1Ac2, a novel cytotoxic crystal protein isolated from Bacillus thuringiensis B0462 strain. Curr Microbiol. 2013;66:475-80. https://doi.org/10.1007/s00284-013-0301-1

Ito A, Sasaguri Y, Kitada S, Kusaka Y, Kuwano K, Masutomi K, et al. A Bacillus thuringiensis crystal protein with selective cytocidal action to human cells. J Biol Chem. 2004;279(20):21282-86. https://doi.org/10.1074/jbc.M401881200

Okumura S, Ishikawa T, Saitoh H, Akao T, Mizuki E. Identification of a second cytotoxic protein produced by Bacillus thuringiensis A1470. Biotechnol Lett. 2013;35:1889-94. https://doi.org/10.1007/s10529-013-1275-6

Hayakawa T, Kanagawa R, Kotani Y, Kimura M, Yamagiwa M, Yamane Y, et al. Parasporin-2Ab, a newly isolated cytotoxic crystal protein from Bacillus thuringiensis. Curr Microbiol. 2007;55:278-83. https://doi.org/10.1007/s00284-006-0351-8

Yamashita S, Katayama H, Saitoh H, Akao T, Park YS, Mizuki E, et al. Typical three-domain cry proteins of Bacillus thuringiensis strain A1462 exhibit cytocidal activity on limited human cancer cells. J Biochem. 2005;138(6):663-72. https://doi.org/10.1093/jb/mvi177

Lee DW, Katayama H, Akao T, Maeda M, Tanaka R, Yamashita S, et al. A 28 kDa protein of the Bacillus thuringiensis serovar shandongiensis isolate 89-T-34-22 induces a human leukemic cell-specific cytotoxicity. Biochim Biophys Acta Protein Struct Mol Enzymol. 2001;1547(1):57-63. https://doi.org/10.1016/S0167-4838(01)00169-8

Paik HD, Bae SS, Park SH, Pan JG. Identification and partial characterization of tochicin, a bacteriocin produced by Bacillus thuringiensis subsp tochigiensis. J Ind Microbiol Biotechnol. 1997;19:294-98. https://doi.org/10.1038/sj.jim.2900462

Cherif A, Ouzari H, Daffonchio D, Cherif H, Ben Slama K, Hassen A, et al. Thuricin 7: a novel bacteriocin produced by Bacillus thuringiensis BMG1. 7, a new strain isolated from soil. Lett Appl Microbiol. 2001;32(4):243-47. https://doi.org/10.1046/j.1472-765X.2001.00898.x

Ahern M. Verschueren S, Van Sinderen D. Isolation and characterisation of a novel bacteriocin produced by Bacillus thuringiensis strain B439. FEMS Microbiol Lett. 2003;220(1):127-31. https://doi.org/10.1016/S0378-1097(03)00086-7

Dong YH, Zhang XF, Xu JL, Zhang LH. Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl Environ Microbiol. 2004;70(2):954-60. https://doi.org/10.1128/AEM.70.2.954-960.2004

Park SJ, Park SY, Ryu CM, Park SH, Lee JK. The role of AiiA, a quorum-quenching enzyme from Bacillus thuringiensis, on the rhizosphere competence. J microbiol biotechn. 2008;18(9):1518-21. https://pubmed.ncbi.nlm.nih.gov/18852506/

De la Fuente-Salcido N, Guadalupe Alanís-Guzmán M, Bideshi DK, et al. Enhanced synthesis and antimicrobial activities of bacteriocins produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol. 2008;190:633-40. https://doi.org/10.1007/s00203-008-0414-2

López-Meza JE. Activity of bacteriocins synthesized by Bacillus thuringiensis against Staphylococcus aureus isolates associated to bovine mastitis. Vet Microbiol. 2009;138(1-2):179-83. https://doi.org/10.1016/j.vetmic.2009.03.018

Kamoun F, Fguira IB, Hassen NBB, Mejdoub H, Lereclus D, Jaoua S. Purification and characterization of a new Bacillus thuringiensis bacteriocin active against Listeria monocytogenes, Bacillus cereus and Agrobacterium tumefaciens. Appl Biochem Biotechnol. 2011;165:300-14. https://doi.org/10.1007/s12010-011-9252-9

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

Ugras S, Demirbag Z. Screening antibacterial activity of entomopathogenic bacteria isolated from pests of hazelnut. Biologia. 2013;68:592-98.

https://doi.org/10.2478/s11756-013-0210-6

Elsharkawy MM, Nakatani M, Nishimura M, Arakawa T, Shimizu M, Hyakumachi M. Control of tomato bacterial wilt and root-knot diseases by Bacillus thuringiensis CR-371 and Streptomyces avermectinius NBRC14893. Acta Agric Scand B Soil Plant Sci. 2015;65(6):575-80. https://doi.org/10.1080/09064710.2015.1031819

Ortiz-Rodríguez T, Mendoza-Acosta F, Martínez-Zavala SA, et al. Thurincin H is a nonhemolytic bacteriocin of Bacillus thuringiensis with potential for applied use. Probiotics Antimicrob Proteins. 2023;15(4):955-66. https://doi.org/10.1007/s12602-022-09952-2

Sadfi N, Cherif M, Fliss I, Boudabbous A, Antoun H. Evaluation of bacterial isolates from salty soils and Bacillus thuringiensis strains for the biocontrol of Fusarium dry rot of potato tubers. J Plant Pathol. 2001;101-17. https://doi.org/10.4454/JPP.V83I2.1118

Kim PI, Bai H, Bai D, Chae H, Chung S, Kim Y, et al. Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol. 2004;97(5):942-49. https://doi.org/10.1111/j.1365-2672.2004.02356.x

Reyes-Ramírez A, Escudero?Abarca BI, Aguilar?Uscanga G, Hayward?Jones PM, Barboza?Corona JE. Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J Food Sci. 2004;69(5):M131-34. https://doi.org/10.1111/j.1365-2621.2004.tb10721.x

Tang Y, Zou J, Zhang L, Li Z, Ma C, Ma N. Anti-fungi activities of Bacillus thuringiensis H3 chitinase and immobilized chitinase particles and their effects to rice seedling defensive enzymes. J Nanosci Nanotechnol. 2012;12(10):8081-86. https://doi.org/10.1166/jnn.2012.6639

Gomaa EZ. Chitinase production by Bacillus thuringiensis and Bacillus licheniformis: their potential in antifungal biocontrol. Korean J Microbiol KJM. 2012;50(1):103-11. https://doi.org/10.1007/s12275-012-1343-y

Kamenek LK, Kamenek DV, Terpilowski MA, Gouli VV. Antifungal action of Bacillus thuringiensis delta-endotoxin against pathogenic fungi related to Phytophthora and Fusarium. J Agric Technol. 2012;8:191-203.

Akram W, Mahboob A, Javed AA. Bacillus thuringiensis strain 199 can induce systemic resistance in tomato against Fusarium wilt. Eur J Microbiol Immunol. 2013;3(4):275-80. https://doi.org/10.1556/eujmi.3.2013.4.7

Zheng M, Shi J, Shi J, Wang Q, Li Y. Antimicrobial effects of volatiles produced by two antagonistic Bacillus strains on the anthracnose pathogen in postharvest mangos. Biol Control. 2013;65(2):200-06. https://doi.org/10.1016/j.biocontrol.2013.02.004

Tao A, Pang F, Huang S, Yu G, Li B, Wang T. Characterisation of endophytic Bacillus thuringiensis strains isolated from wheat plants as biocontrol agents against wheat flag smut. Biocontrol Sci Techn. 2014;24(8):901-24.

https://doi.org/10.1080/09583157.2014.904502

Rocha LO, Tralamazza SM, Reis GM, Rabinovitch L, Barbosa CB, Corrêa B. Multi-method approach for characterizing the interaction between Fusarium verticillioides and Bacillus thuringiensis subsp. kurstaki. PLoS One. 2014;9(4):e92189. https://doi.org/10.1371/journal.pone.0092189

Shrestha A, Sultana R, Chae JC, Kim K, Lee KJ. Bacillus thuringiensis C25 which is rich in cell wall degrading enzymes efficiently controls lettuce drop caused by Sclerotinia minor. Eur J Plant Pathol. 2015;142:577-89. https://doi.org/10.1007/s10658-015-0636-5

Hollensteiner J, Wemheuer F, Harting R, Kolarzyk AM, et al. Bacillus thuringiensis and Bacillus weihenstephanensis inhibit the growth of phytopathogenic Verticillium species. Front Microbiol. 2017;7:2171. https://doi.org/10.3389/fmicb.2016.02171

Choi TG, Maung CEH, Lee DR, Henry AB, Lee YS, Kim KY. Role of bacterial antagonists of fungal pathogens, Bacillus thuringiensis KYC and Bacillus velezensis CE 100 in control of root-knot nematode, Meloidogyne incognita and subsequent growth promotion of tomato. Biocontrol Sci Techn. 2020;30(7):685-700. https://doi.org/10.1080/09583157.2020.1765980

He CN, Ye WQ, Zhu YY, Zhou WW. Antifungal activity of volatile organic compounds produced by Bacillus methylotrophicus and Bacillus thuringiensis against five common spoilage fungi on loquats. Mol. 2020;25(15):3360. https://doi.org/10.3390/molecules25153360

Azizoglu ZB, Yilmaz S, Azizoglu U, Karabörklü S, Temizgul R, Ayvaz A. Molecular characterization of the chitinase genes of native Bacillus thuringiensis isolates and their antagonistic activity against three important phytopathogenic fungi. Biologia. 2021;76(9):2745-55. https://doi.org/10.1007/s11756-021-00802-0

Amallia R, Suryanti S, Joko T. The potential of Rhizophagus intraradices, Bacillus thuringiensis Bt BMKP and silica for anthracnose disease control in shallot. J Sustain Agric. 2023;38(2):433-46. 10.20961/carakatani.v38i2.76536

Ünlü E, Çal?? Ö, Say A, Karim AA, Yeti?ir H, Y?lmaz S. Investigation of the effects of Bacillus subtilis and Bacillus thuringiensis as bio-agents against powdery mildew (Podosphaera xanthii) disease in zucchini (Cucurbita pepo L.). Microb Pathog. 2023;185:106430. https://doi.org/10.1016/j.micpath.2023.106430

Kadjo AC, Beugre GC, Kone KM, Kedjebo KBD, Mounjouenpou P, Durand N, et al. Effect of the improvement of cocoa raw material quality by application of anti-fungal Bacillus strains during fermentation on the chocolate sensory attributes. In: Research Advances and Challenges in Agricultural Sciences. B P International. 2024;83-99. https://doi.org/10.9734/bpi/racas/v2/7129C

Bai Y, Zhou X, Smith DL. Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci. 2003;43(5):1774-81. https://doi.org/10.2135/cropsci2003.1774

Sheikh LI, Dawar shahnaz, Zaki MJ, Ghaffar A. Efficacy of Bacillus thuringiensis and Rhizobium meliloti with nursery fertilizers in the control of root infecting fungi on mung bean and okra plants. Pak J Bot. 2006;38(2):465.

Lee KD, Gray EJ, Mabood F, Jung WJ, Charles T, Clark SR, et al. The class IId bacteriocin thuricin-17 increases plant growth. Planta. 2009;229:747-55. https://doi.org/10.1007/s00425-008-0870-6

Praca LB, Gomes ACMM, Cabral G, Martins ES, Sujii EH Monnerat RG. Endophytic colonization by Brazilian strains of Bacillus thuringiensis on cabbage seedlings grown in vitro. Bt Research. 2012;3(3):11-19. https://doi.org/10.5376/bt.2012.03.0003

Ahmed EA, Hassan EA, El Tobgy KMK, Ramadan EM. Evaluation of rhizobacteria of some medicinal plants for plant growth promotion and biological control. Ann Agric Sci. 2014;59(2):273-80. https://doi.org/10.1016/j.aoas.2014.11.016

Armada E, Azcón R, López-Castillo OM, Calvo-Polanco M, Ruiz-Lozano JM. 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. J Plant Biochem Physiol. 2015;90:64-74. https://doi.org/10.1016/j.plaphy.2015.03.004

Ortiz N, Armada E, Duque E, Roldán A, Azcón R. 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. 2015;174:87-96. https://doi.org/10.1016/j.jplph.2014.08.019

Prudent M, Salon C, Souleimanov A, Emery RN, Smith DL. Soybean is less impacted by water stress using Bradyrhizobium japonicum and thuricin-17 from Bacillus thuringiensis. Agron Sustain Dev. 2015;35:749-57. https://doi.org/10.1007/s13593-014-0256-z

Rojas-Solís D, Hernández-Pacheco CE, Santoyo G. Evaluation of Bacillus and Pseudomonas to colonize the rhizosphere and their effect on growth promotion in tomato (Physalis ixocarpa Brot. ex Horm.). Rev Chapingo Ser Hortic. 2016;22(1):45-58. https://doi.org/10.5154/r.rchsh.2015.06.009

Armada E, Probanza A, Roldán A, Azcón R. 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. 2016;192:1-12. https://doi.org/10.1016/j.jplph.2015.11.007

Cherif-Silini H, Silini A, Yahiaoui B, Ouzari I, Boudabous A. Phylogenetic and plant-growth-promoting characteristics of Bacillus isolated from the wheat rhizosphere. Ann Microbiol. 2016;66(3):1087-97. https://doi.org/10.1007/s13213-016-1194-6

Bandopadhyay S. Application of plant growth promoting Bacillus thuringiensis as biofertilizer on Abelmoschus esculentus plants under field condition. J Pure Appl Microbiol. 2020;14(2):1287-94. https://doi.org/10.22207/JPAM.14.2.24

Khan N, Bano AM, Babar A. Impacts of plant growth promoters and plant growth regulators on rainfed agriculture. PloS One. 2020;15(4):e0231426. https://doi.org/10.1371/journal.pone.0231426

Shah AA, Bibi F, Hussain I, Yasin NA, Akram W, Tahir MS, et al. Synergistic effect of Bacillus thuringiensis iags 199 and putrescine on alleviating cadmium-induced phytotoxicity in Capsicum annum. Plants. 2020;9(11):1512. https://doi.org/10.3390/plants9111512

de Almeida JR, Bonatelli ML, Batista BD, Teixeira?Silva NS, Mondin M, Dos Santos RC, et al. Bacillus thuringiensis RZ2MS9, a tropical plant growth?promoting rhizobacterium, colonizes maize endophytically and alters the plant's production of volatile organic compounds during co?inoculation with Azospirillum brasilense Ab?V5. Environ Microbiol Rep. 2021;13(6):812-21. https://doi.org/10.1111/1758-2229.13004

Asgharzadeh A, Saghafi K, Fattahifar E, Jenaghi M, Alizadeh N. Stimulatory effect of plant growth promoter bacteria on in vitro culture of Agaricus bisporus mushroom and bio controlling effect on pathogenic fungi. J Soil Biol. 2024;11(2):139-54. https://doi.org/10.22092/SBJ.2024.361318.245

Published

02-12-2024

How to Cite

1.
Vignesh S, Rajadurai G, Raghu R, Balakrishnan N, Jayakanthan M, Mohankumar S. Potential applications of Bacillus thuringiensis Berliner in agriculture, medicine and environment. Plant Sci. Today [Internet]. 2024 Dec. 2 [cited 2024 Dec. 22];11(sp4). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/3977

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