Research Progress on the Safety of Bacillus thuringiensis

doi:10.16409/j.cnki.2095-039x.2021.01.022

Abstract

Abstract: Bacillus thuringiensis (Bt) has become the most widely used type of microbial pesticide. This review summarized the registration and safety evaluation of Bt products in China and the United States, and analyzed the risk evaluation of Bt products. Bt strains are not known pathogens of humans or other mammals, and non-toxic, infectious and pathogenic to mammals, poultry, etc.; their populations gradually decreased in the environment, and there is no residual risk; it has no significant impact on the survival and reproduction of non-target insects and the structure of soil microbial community.

Key words: Bacillus thuringiensis, microbial pesticide, registration, safety assessment

CLC Number:

S476.1

GENG Lili, TAO Lingmei, ZHANG Hongjun, ZAHNG Jie. Research Progress on the Safety of Bacillus thuringiensis[J]. Chinese Journal of Biological Control, 2021, 37(1): 2-10.

References

[1] Ishiwata S. On a kind of severe flacherie (sotto disease)[J]. Dainihon Sanshi Kaiho, 1901, 114(1):5.
[2] Berliner E. Über die Schlaffsucht der Mehlmottenraupe (Ephestia kühniella Zell.) und ihren erreger Bacillus thuringiensis n. sp[J]. Zeitschrift für Angewandte Entomologie, 1915, 2(1):29-56.
[3] Soberon M, Gill S S, Bravo A. Signaling versus punching hole:how do Bacillus thuringiensis toxins kill insect midgut cells?[J].Cellular and Molecular Life Sciences, 2009, 66:1337-1349.
[4] Bravo A, Likitvivatanavong S, Gill S, et al. Bacillus thuringiensis:A story of a successful bioinsecticide[J]. Insect Biochemistry and Molecular Biology, 2011, 41:423-431.
[5] James C. Global Status of Commercialized Biotech/GM Crops:2018. ISAAA Brief No.54[M]. Ithaca, NY:ISAAA, 2019
[6] Arthurs S, Dara S K. Microbial biopesticides for invertebrate pests and their markets in the United States[J]. Journal of Invertebrate Pathology, 2019, 165:13-21.
[7] 张文君. 美国生物农药登记管理情况[J]. 农药科学与管理, 2002, 23(2):43-44.
[8] 施天柱, 张碧海, 林艳, 等. 苏云金杆菌杀虫剂的特点及应用[J]. 新疆农垦科技, 2006(4):50-51.
[9] 刘志勇, 李启富, 周银平, 等. 苏云金杆菌的急性毒性及致敏实验观察[J]. 上海实验动物科学, 2004(3):35-37.
[10] 黄光全, 陈国英, 李松增, 等. 苏云金杆菌以色列变种"187"株对哺乳动物急性安全试验[J]. 公共卫生与预防医学, 2000(2):35-36.
[11] 陈国英, 黄光全, 李松增, 等. 苏云金杆菌以色列变种187株对哺乳动物亚急性毒性试验[J]. 公共卫生与预防医学, 1999(6):59-60.
[12] 黄光全, 徐博钊, 李松增, 等. 苏云金杆菌以色列变种187株对鱼类及水生动物毒性试验[J]. 湖北预防医学杂志, 2000(1):39-40.
[13] 陈波, 谷明娟, 朱遥, 等. 苏云金芽胞杆菌BtZ01对小鼠胚胎和胚后发育的影响[J]. 生态毒理学报, 2015, 10(2):325-331.
[14] Xu W, Cao S, He X, et al. Safety assessment of Cry1Ab/Ac fusion protein[J]. Food and Chemical Toxicology, 2009, 47(7):1459-1465.
[15] Wang G, Zhang J, Song F, et al. Engineered Bacillus thuringiensis G033A with broad insecticidal activity against Lepidopteran and Coleopteran pests[J]. Applied Microbiology and Biotechnology, 2006, 72:924-930.
[16] 张杰. 转cry3Aa基因苏云金芽胞杆菌G033A的安全证书申报书. 2019.
[17] Mancebo A, Molier T, González B, et al. Acute oral, pulmonary and intravenous toxicity/pathogenicity testing of a new formulation of Bacillus thuringiensis var israelensis SH-14 in rats[J]. Regulatory Toxicology and Pharmacology, 2011, 59(1):184-190.
[18] Wang C, Li W, Kessenich C R, et al. Safety of the Bacillus thuringiensis-derived Cry1A. 105 protein:Evidence that domain exchange preserves mode of action and safety[J]. Regulatory Toxicology and Pharmacology, 2018, 99:50-60.
[19] EFSA Biohazard Panel. Risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs[J]. EFSA Journal, 2016, 14:99.
[20] Raymond B, Federici B A. In defense of Bacillus thuringiensis, the safest and most successful microbial insecticide available to humanity-a response to EFSA[J]. FEMS Microbiology Ecology, 2017, 93:7.
[21] Siegel J P. The Mammalian safety of Bacillus thuringiensis-based insecticides[J]. Journal of Invertebrate Pathology, 2001, 77(1):13-21.
[22] West A W, Burges H D, Dixon T J, et al. Survival of Bacillus thuringiensis and Bacillus cereus spore inoculation in soil:effects of pH, moisture, nutrient availability and indigenous microorganisms[J]. Soil Biology and Biochemistry, 1985, 17(5):657-665.
[23] Petras S F, Casida L E. Survival of Bacillus thuringiensis spores in soil[J]. Applied and Environmental Microbiology, 1986, 50(6):1496-1501.
[24] Pruett C J H, Burges H D, Wyborn C H. Effect of exposure to soil on potency and spore viability of Bacillus thuringiensis[J]. Journal of Invertebrate Pathology, 1980, 35(2):168-174.
[25] 黄威, 张运红, 陈迪勤, 等. Bt蛋白在几种土壤中的降解与残留[J]. 华中农业大学学报, 2009, 28(2):51-55.
[26] 黄冠辉, 邵冬梅, 王卫国, 等. 苏云金杆菌芽胞在作物叶面和土壤中的存活期研究[J]. 微生物学通报, 1981(1):7-9.
[27] Wang X, Xue Y, Han M, et al. The ecological roles of Bacillus thuringiensis within phyllosphere environments[J]. Chemosphere, 2014, 108:258-264.
[28] Schoenly K G, Cohen M B, Barrion A T, et al. Effects of Bacillus thuringiensis on non-target herbivore and natural enemy assemblages in tropical irrigated rice[J]. Environmental Biosafety Research, 2003, 2(3):181-206.
[29] Stefan R, Eva S, Heinz H, et al. Diabrotica-resistant Bt maize DKc5143 event MON88017 has no impact on the field densities of the leafhopper Zyginidia scutellaris[J]. Environmental Biosafety Research, 2010, 9:87-99.
[30] Dutton A, Klein H, Romeis J, et al. Prey-mediated effects of Bacillus thuringiensis spray on the predator Chrysoperla carnea in maize[J]. Biological Control, 2003, 26(2):209-215.
[31] Romeis J, Dutton A, Bigler F. Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera:Chrysopidae)[J]. Journal of Insect Physiology, 2004, 50(2-3):175-183.
[32] 王广君. 高效广谱苏云金芽孢杆菌工程菌的构建及杀虫晶体蛋白的研究[D]. 北京:中国农业科学院, 2005.
[33] Lu H, Rajamohan F, Dean D H. Identification of amino acid residues of Bacillus thuringiensis delta-endotoxin CryIAa associated with membrane binding and toxicity to Bombyx mori[J]. Journal of Bacteriology, 1994, 176(17):5554-5559.
[34] Liu Y, Zhou Z, Wang Z, et al. Replacement of loop2 and 3 of Cry1Ai in domain II affects specificity to the economically important insect Bombyx mori[J]. Journal of invertebrate pathology, 2020, 169:107296.
[35] Jiao Y, Yang Y, Meissle M, et al. Comparison of susceptibility of Chilo suppressalis and Bombyx mori to five Bacillus thuringiensis proteins[J]. Journal of Invertebrate Pathology, 2016, 136:95-99.
[36] 赵旭, 叶幸, 张燕, 等. 3种典型微生物农药对家蚕的毒性研究[J]. 生态毒理学报, 2017, 12(4):219-226.
[37] 袁志东, 姚洪渭, 叶恭银, 等. 转Bt基因水稻花粉对家蚕不同品种幼虫的生存分析[J]. 蚕桑通报, 2006, 3:23-27.
[38] Babendreier D, Kalberer N M, Fluri P, et al. Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees[J]. Apidologie, 2005, 36:585-594.
[39] Sims S R. Bacillus thuringiensis var. kurstaki CryIA (c) protein expressed in transgenic cotton:effects on beneficial and other non-target insects[J]. Southwestern Entomology, 1995, 20:493-500.
[40] Malone L A, Burgess E P J, Gatehouse H S, et al. Effects of ingestion of a Bacillus thuringiensis toxin and a trypsin inhibitor on honey bee flight activity and longevity[J]. Apidologie, 2001, 32(1):57-68.
[41] 田岩, 张永军, 吴孔明, 等. 转Bt-cry1Ab玉米花粉对意大利蜜蜂生长发育及体内酶活性的影响[J]. 农业生物技术学报, 2006, 14(6):990-991.
[42] Babendreier D, Joller D, Romeis J, et al. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins[J]. FEMS Microbiology Ecology, 2007, 59:600-610.
[43] Dai P, Wang M, Geng L, et al. The effect of Bt Cry9Ee toxin on honey bee brood and adults reared in vitro, Apis mellifera (Hymenoptera:Apidae)[J]. Ecotoxicology and Environmental Safety, 2019, 181:381-387.
[44] Jiang W, Geng L, Dai P, et al. The Influence of Bt-transgenic maize pollen on the bacterial diversity in the midgut of Chinese honeybees, Apis cerana cerana[J]. Journal of Integrative Agriculture, 2013, 12(3):474-482.
[45] Geng L, Cui H, Dai P, et al. The influence of Bt-transgenic maize pollen on the bacterial diversity in the midgut of Apis mellifera ligustica[J]. Apidologie, 2013, 44:198-208.
[46] Dhillon M K, Sharma H C. Effects of Bacillus thuringiensis δ-endotoxins Cry1Ab and Cry1Ac on the coccinellid beetle, Cheilomenes sexmaculatus (Coleoptera, Coccinellidae) under direct and indirect exposure conditions[J]. Biocontrol Science and Technology, 2009, 19(4):407-420.
[47] Duan J J, Head G, McKee M J, et al. Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bb1 protein on a non-target ladybird beetle, Coleomegilla maculate[J]. Entomologia Experimentalis et Applicata, 2002, 104:271-280.
[48] Koskella J, Stotzky G. Larvicidal toxins from Bacillus thuringiensis subspp. kurstaki, morrisoni, (strain tenebrionis), and israelensis, have no microbicidal or microbiostatic activity against selected bacteria, fungi, and algae in vitro[J]. Canadian Journal of Microbiology, 2002, 48(3):262-267.
[49] 韩美哲, 王小显, 刘常宏, 等. 苏云金芽胞杆菌菌剂对棉花根际土壤细菌数量及多样性的影响[J]. 中国生态农业学报, 2013, 21(10):109-115.
[50] 冯书亮, 范秀华, 王容燕, 等. 苏云金杆菌在华北果园土壤中消长动态的研究[J]. 中国病毒学, 2000(S1):110-114.
[51] Li Z, Bu N, Chen C, et al. Soil incubation studies with Cry1Ac protein indicate no adverse effect of Bt crops on soil microbial communities[J]. Ecotoxicology and Environmental Safety, 2018, 152:33-41.
[52] Tan F, Wang J, Feng Y, et al. Bt corn plants and their straw have no apparent impact on soil microbial communities[J]. Plant & Soil, 2010, 329(s1-2):349-364.
[53] 任馨, 吴伟祥, 叶庆富, 等. 转Bt基因克螟稻秸杆对淹水土壤细菌群落的影响[J]. 环境科学学报, 2004, 24(5):871-877.
[54] Vivas A, Marulanda A, Gómez M, et al. Physiological characteristics (SDH and ALP activities) of arbuscular mycorrhizal colonization as affected by Bacillus thuringiensis inoculation under two phosphorus levels[J]. Soil Biology and Biochemistry, 2003, 35(7):987-996.
[55] Armada E, Azcón R, López-Castillo O M, et al. 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 Physiology Biochemstry, 2015, 90:64-74.
[56] 熊鹂, 刘培磊, 徐琳杰, 等. 浅析转基因舆情[J]. 生物安全学报, 2014, 23(4):305-308.
[57] Melo A L A, Soccol V T, Soccol C R. Bacillus thuringiensis:mechanism of action, resistance, and new applications:a review[J]. Critical Reviews in Biotechnology, 2016, 36(2):317-326.
[58] Tabashnik B E, Cushing N L, Finson N, et al. Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera:Plutellidae)[J]. Journal of Economic Entomology, 1990, 83(5):1671-1676.
[59] 戴承镛, 殷向东, 徐熙, 等. 小菜蛾对苏云金杆菌制剂的抗药性及其对策[J]. 中国生物防治学报, 1994, 10(2):62-66.
[60] Tabashnik B E, Gassman A J, Crowdwer D W, et al. Insect resistance to Bt crops:evidence versus theory[J]. Nature Biotechnology, 2008, 26:199-202.
[61] 袁善奎, 刘亮, 王以燕, 等. 农药非法添加隐性成分及其风险分析[J]. 农药, 2016, 7:480-482.