Skip to main content
Log in

Current trends in Bt crops and their fate on associated microbial community dynamics: a review

  • Special Issue: Cell Biology in Agricultural and Food Science
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Cry protein expressing insect-resistant trait is mostly deployed to control major devastating pests and minimize reliance on the conventional pesticides. However, the ethical and environmental issues are the major constraints in their acceptance, and consequently, the cultivation of genetically modified (GM) crops has invited intense debate. Since root exudates of Bacillus thuringiensis (Bt) crops harbor the insecticidal protein, there is a growing concern about the release and accumulation of soil-adsorbed Cry proteins and their impact on non-target microorganisms and soil microbial processes. This review pertains to reports from the laboratory studies and field trials to assess the Bt toxin proteins in soil microbes and the processes determining the soil quality in conjunction with the existing hypothesis and molecular approaches to elucidate the risk posed by the GM crops. Ecological perturbations hinder the risk aspect of soil microbiota in response to GM crops. Therefore, extensive research based on in vivo and interpretation of results using high-throughput techniques such as NGS on risk assessment are imperative to evaluate the impact of Bt crops to resolve the controversy related to their commercialization. But more studies are needed on the risk associated with stacked traits. Such studies would strengthen our knowledge about the plant-microbe interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ahmad A, Wilde GE, Zhu KY (2005) Detectability of coleopteran-specific Cry3Bb1 protein in soil and its effect on nontarget surface and below-ground arthropods. Environ Entomol 34(2):385–394

    Article  CAS  Google Scholar 

  • Al-Kaisi MM, Guzman JG (2013) Effects of tillage and nitrogen rate on decomposition of transgenic Bt and near-isogenic non-Bt maize residue. Soil Till Res 129:32–39

    Article  Google Scholar 

  • Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19(24):5555–5565

    Article  CAS  PubMed  Google Scholar 

  • Badea EM, Chelu F, Lăcătuşu A (2010) Results regarding the levels of Cry1Ab protein in transgenic corn tissue (MON810) and the fate of Bt protein in three soil types. Rom Biotechnol Lett 15:55–62

    CAS  Google Scholar 

  • Bartram AK, Lynchm MD, Stearns JC, Hagelsieb GM, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end Illumina reads. Appl Environ Microbiol 77(11):3846–3852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumgarte S, Tebbe CC (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810), and its effect on bacterial communities in the maize rhizosphere. Mol Ecol 14(8):2539–2551

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68(1):1–13

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51(2):215–229

    Article  CAS  PubMed  Google Scholar 

  • Beura K, Rakshit A (2013) Bt cotton influencing enzymatic activities under varied soils. Open J Ecol 3(08):505–509

  • Blackwood BC, Buyer JS (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J Environ Qual 33(3):832–836

    Article  CAS  PubMed  Google Scholar 

  • Brimecombe MJ, De Leij FA, Lynch JM (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel-Dekker, New York, pp 95–140

    Google Scholar 

  • Brusetti L, Francia P, Bertolini C, Pagliuca A, Borin S, Sorlini C, Abruzzese A et al (2004) Bacterial communities associated with the rhizosphere of transgenic Bt-176 maize (Zea mays) and its non transgenic counterpart. Plant Soil 266(1–2):11–21

    CAS  Google Scholar 

  • Caporasoa G, Lauberb Walters WA, Berg-Lyons D, Huntley J, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 1:4516–4522

    Article  Google Scholar 

  • Castaldini M, Turrini A, Sbrana C, Benedetti A, Machionni M, Mocali S, Fabiani A et al (2005) Impact of Bt corn on rhizosphere rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 71(11):6719–6729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeke TE, Pace BA, Rosenstiel TN, Cruzan MB (2011) The influence of fertilizer level and spore density on arbuscular mycorrhizal colonization of transgenic Bt 11 maize (Zea mays) in experimental microcosms. FEMS Microbiol Ecol 75(2):304–312

    Article  CAS  PubMed  Google Scholar 

  • Cheeke TE, Rosenstiel TN, Cruzan MB (2012) Evidence of reduced arbuscular mycorrhizal fungal colonization in multiple lines of Bt maize. Am J Bot 99(4):700–707

    Article  PubMed  Google Scholar 

  • Cheeke TE, Cruzan MB, Rosenstiel TN (2013) Field evaluation of arbuscular mycorrhizal fungal colonization in Bacillus thuringiensis toxin-expressing (Bt) and non-Bt maize. Appl Environ Microbiol 79(13):4078–4086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZH, Chen LJ, ZhangYL WZJ (2011) Microbial properties, enzyme activities and the persistence of exogenous proteins in a soil under consecutive cultivation of transgenic cotton (Gossypium hirsutum L.). Plant Soil Environ 57(2):67–74

    Google Scholar 

  • Chen ZH, Chen LJ, Wu ZJ (2012) Relationships among persistence of Bacillus thuringiensis and Cowpea trypsin inhibitor proteins, microbial properties and enzyme activities in rhizosphere soil after repeated cultivation with transgenic cotton. Appl Soil Ecol 53:23–30

    Article  Google Scholar 

  • Chun YJ, Kim HJ, Park KW, Jeong SC, Lee B, Back K, Kim HM et al (2012) Two-year field study shows little evidence that PPO-transgenic rice affects the structure of soil microbial communities. Biol Fert Soils 48(4):453–461

    Article  Google Scholar 

  • Ciccazzo S, Esposito A, Rolli E, Zerbe S, Daffonchio D, Brusetti L (2014) Safe-site effects on rhizosphere bacterial communities in a high-altitude alpine environment. ID 480170 doi.org/10.1155/2014/480170

  • 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 

  • Das NR, Chaudhary R, Joshi HC (2009) Detection and persistence of Bt toxin in decomposition study of Bt leaves of transgenic cotton. J Environ Res Dev 3(3):859–866

    CAS  Google Scholar 

  • Daudu CK, Muchaonyerwa P, Mnkeni PNS (2009) Litterbag decomposition of genetically modified maize residues and their constituent Bacillus thuringiensis protein (Cry1Ab) under field conditions in the central region of the Eastern Cape, South Africa. Agr Ecosys Environ 134(3–4):153–158

    Article  CAS  Google Scholar 

  • de Souza Vieira PD, de Souza Motta CM, Lima D, Torres JB, Quecine MC, Azevedoc JL, de Oliveira NT (2011) Endophytic fungi associated with transgenic and non-transgenic cotton. Mycology 2(2):91–97

    Article  Google Scholar 

  • de Vaufleury A, Kramarz PE, Binet P, Cortet J, Cauld S, Andersen MN, Plumey E et al (2007) Exposure and effects assessments of Bt-maize on non-target organisms (gastropods, microarthropods, mycorrhizal fungi) in microcosms. Pedobiologia 51:185–194

    Article  CAS  Google Scholar 

  • Delmont TO, Malandain C, Prestat E, Larose C, Monier JM, Simonet P, Vogel TM et al (2011) Metagenomic mining for microbiologists. ISME J 5(12):1837–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Schrijver A, Devos Y, Van Den Bulke M, Cadot P, De Loose M, Reheul D, Sneyers M (2007) Risk assessment of GM stacked events obtained from crosses between GM events. Trends in Food Sci Technol 18(2):101–109

    Article  CAS  Google Scholar 

  • Devare MH, Jones CM, Thies JE (2004) Effect of Cry3Bb transgenic corn and tefluthrin on the soil microbial community: biomass, activity, and diversity. J Environ Qual 33(3):837–843

    Article  CAS  PubMed  Google Scholar 

  • Devare M, Londono RLM, Thies JE (2007) Neither transgenic Bt maize (MON 63) nor tefluthrin insecticides adversely affect soil microbial activity or biomass: a 3-year field analysis. Soil Biol Biochem 39:2038–2038

    Article  CAS  Google Scholar 

  • Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L, Hatay M et al (2008) Microbial ecology of four coral atolls in the northern line islands. PLoS One 3(2), e1584

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dohrmann AB, Küting M, Jünemann S, Jaenicke S, Schlüter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt- and conventional maize varieties. ISME J 7:37–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Donegan KK, Palm CJ, Fieland VJ, Porteous LA, Ganio LM, Schaller DL (1995) Changes in levels, species, and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Appl Soil Ecol 2(2):111–124

    Article  Google Scholar 

  • Donegan KK, Shaller DL, Stone JK, Ganio LM, Reed G, Hamm PB, Seidler RJ (1996) Microbial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var. tenebrionis endotoxin. Transg Res 5(1):25–35

    Article  CAS  Google Scholar 

  • Dong HZ, Li WJ (2007) Variability of endotoxin expression in Bt transgenic cotton. J Agron Crop Sci 193(1):21–29

    Article  CAS  Google Scholar 

  • Dubelman S, Ayden BR, Bader BM, Brown CR, Jiang C, Vlachos D (2005) Cry1Ab protein does not persist in soil after 3 years of sustained Bt corn use. Environ Entomol 34(4):915–921

    Article  CAS  Google Scholar 

  • Dutta D, Gopal M, Shukla L, Mahajan VK (2012) Evaluating safety of genetically modified crops: effect of Bt-transgenic cabbage plants on microbial dynamics and dehydrogenase activity. Indian J Agri Sci 82(6):552

    Google Scholar 

  • Fang M, Kremer RJ, Motavalli PP, Davis G (2005) Bacterial diversity in rhizospheres of nontransgenic and transgenic corn. Appl Environ Microbiol 71(7):4132–4136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang M, Motavalli PP, Kremer RJ, Nelson KA (2007) Assessing changes in soil microbial communities and carbon mineralization in Bt and non-Bt corn residue-amended soils. Appl Soil Ecol 37(1–2):150–160

    Article  Google Scholar 

  • Fang H, Dong B, Yan H, Tang F, Wang B, Yu Y (2012) Effect of vegetation of transgenic Bt rice lines and their straw amendment on soil enzymes, respiration, functional diversity and community structure of soil microorganisms under field conditions. J Environ Sci 24(7):1259–1270

    Article  CAS  Google Scholar 

  • Feng Y, Ling L, Fan H, Liu Y, Tan F, Shu Y, Wang J (2011) Effects of temperature, water content and pH on degradation of Cry1Ab protein released from Bt corn straw in soil. Soil Biol Biochem 43(7):1600–1606

    Article  CAS  Google Scholar 

  • Ferreira LHPL, Molina JC, Brasil C, Andrade G (2003) Evaluation of Bacillus thuringiensis bioinsecticidal protein effects on soil microorganisms. Plant Soil 256(1):161–168

    Article  CAS  Google Scholar 

  • Fitter (2012) Why plant science matters. New Phytol 193 (1): 1–12

  • Flieβbach A, Messmer M, Nietlispach B, Infante V, Mader P (2012) Effects of conventionally bred and Bacillus thuringiensis (Bt) maize varieties on soil microbial biomass and activity. Biol Fert Soils 48(3):315–324

    Article  CAS  Google Scholar 

  • Flores S, Saxena D, Stotzky G (2005) Transgenic Bt plants decompose less in soil than non-Bt plants. Soil Biol Biochem 37(6):1073–1082

    Article  CAS  Google Scholar 

  • Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, Macphee R (2010) Microbiome profiling by Illumina sequencing of combinatorial sequence-tagged PCR products. Plos One 5(10), e15406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Griffiths BS, Caul S, Thompson J, Birch ANE, Scrimeour C, Cortet J, Foggo A et al (2006) Soil microbial and faunal community responses to Bt-maize and insecticide in two soils. J Environ Qual 35(3):734–741

    Article  CAS  PubMed  Google Scholar 

  • Griffiths BS, Caul S, Thompson J, Birch ANE, Cortet J, Anderson MN, Krogh PH (2007) Microbial and microfaunal community structure in cropping systems with genetically modified plants. Pedobiol 51(3):195–206

    Article  Google Scholar 

  • Hannula SE, Boschker HTS, de Boer W, van Veen JA (2012) 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytol 194(3):784–799

    Article  CAS  PubMed  Google Scholar 

  • Head G, Surber JB, Watson JA, Martin JW, Duan JJ (2002) No detection of Cry1Ac protein in soil after multiple years of transgenic Bt cotton (Bollgard) use. Environ Entomol 31(1):30–36

    Article  CAS  Google Scholar 

  • Helassa N, Quiquampoix H, Noinville S, Szponarski W, Staunton S (2009) Adsorption and desorption of monomeric Bt (Bacillus thuringiensis) Cry1Aa toxin on montmorillonite and kaolinite. Soil Biol Biochem 41(3):498–504

    Article  CAS  Google Scholar 

  • Hendriksma HP, Härtel S, Babendreier D, von der OheW DIS (2012) Effects of multiple Bt proteins and GNA lectin on in vitro-reared honey bee larvae. Apidologie 43(5):549–560

    Article  CAS  Google Scholar 

  • Heuer H, Kroppenstedt RM, Lottmann J, Berg G, Smalla K (2002) Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl Environ Microbiol 68(3):1325–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hopkins DW, Gregorich EG (2003) Detection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize. Europ J Soil Sci 54(4):793–800

    Article  Google Scholar 

  • Hu HY, Liu XX, Zhao ZW, Sun JG, Zhang QW, Liu XZ, Yu Y (2009) Effects of repeated cultivation of transgenic Bt cotton on functional bacterial populations in rhizosphere soil. World J Microbiol Biotechnol 25(3):357–366

    Article  CAS  Google Scholar 

  • Hur M, Kim Y, Song HR, Kim JM, Choi YI, Yi H (2011) Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings. Appl Microbiol Ecol 77(21):7611–7619

    CAS  Google Scholar 

  • Hussain Q, Liu Y, Zhang A, Pan G, Li Z, Zhang X, Song X et al (2011) Variation of bacterial and fungal community structures in the rhizosphere of hybrid and standard rice cultivars and linkage to CO2 flux. FEMS Microbiol Ecol 78(1):116–128

    Article  CAS  PubMed  Google Scholar 

  • Icoz I, Stotzky G (2008a) Cry3Bb1 protein from Bacillus thuringiensis in root exudates and biomass of transgenic corn does not persist in soil. Transgenic Res 17(4):609–620

    Article  CAS  PubMed  Google Scholar 

  • Icoz I, Stotzky G (2008b) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40(3):559–586

    Article  CAS  Google Scholar 

  • Icoz I, Saxena D, Andow D, Zwahlen C, Stotzky G (2008) Microbial populations and enzyme activities in soil in situ under transgenic corn expressing Cry proteins from Bacillus thuringiensis. J Environ Qual 37(2):647–662

    Article  CAS  PubMed  Google Scholar 

  • ISAAA Pocket K No. 42: Stacked traits in biotech crops. ISAAA, Ithaca

  • James C (2014) Global status of commercialized biotech/GM crops: 2014. ISAAA Brief No. 49. ISAAA: Ithaca, NY

  • Johnson KL, Raybould AJ, Hudson MD, Poppy GM (2006) How does scientific risk assessment of GM crops fit within the wider risk analysis? Trends Plant Sci 12:1–5

    Article  PubMed  CAS  Google Scholar 

  • Jung S, Park S, Kim D, Kim SB (2008) Denaturing gradient gel electrophoresis analysis of bacterial community profiles in the rhizosphere of cry1Ac-carrying Brassica rapa subsp. pekinensis. J Microbiol 46(1):12–15

    Article  CAS  PubMed  Google Scholar 

  • Kapur M, Bhatia R, Pandey G, Pandey J, Paul D (2010) A case study for assessment of microbial community in crop fields. Curr Microbiol 61(2):118–124

    Article  CAS  PubMed  Google Scholar 

  • Knief C (2014) Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front Plant Sci. doi:10.3389/fpls.2014.00216

    PubMed  PubMed Central  Google Scholar 

  • Knox OGG, Nehl DB, Mor T, Roberts GN, Gupta VVSR (2008) Genetically modified cotton has no effect on arbuscular mycorrhizal colonisation of roots. Field Crops Res 109(1–3):57–60

    Article  Google Scholar 

  • Koskella J, Stotzky G (2002) 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. Can J Microbiol 48(3):262–267

    Article  CAS  PubMed  Google Scholar 

  • Kravchenko AN, Hao X, Robertson GP (2009) Seven years of continuously planted Bt corn did not affect mineralizable and total soil C and total N in surface soil. Plant Soil 318:269–274

    Article  CAS  Google Scholar 

  • Kuramae EE, Verbruggen E, Hillekens R, de Hollander M, Roling WFM, van der Heijden MGA, Kowalchuk A (2013) Tracking fungal community responses to maize plants by DNA- and RNA-based pyrosequencing. PLoS One 8(7), e69973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol Pers 19(7):792–798

    Article  CAS  Google Scholar 

  • Lang A, Arndt M, Beck R, Bauchhenss J, Pommer G (2006) Monitoring of the environmental effects of the Bt gene. Bavarian State Research Center for Agriculture No. 2006/10. Vo¨ttinger Strasse 38, 85354 Freising-Weihenstephan

  • Lawhorn CN, Neher DA, Dively GP (2009) Impact of coleopteran targeting toxin (Cry3Bb1) of Bt corn on microbially mediated decomposition. Appl Soil Ecol 41(3):364–368

    Article  Google Scholar 

  • Lee SH, Kimi CG, Kang H (2011) Temporal dynamics of bacterial and fungal communities in a genetically modified (GM) rice ecosystem. Microb Ecol 61(3):646–659

    Article  PubMed  Google Scholar 

  • Lehman RM, Osborne SL, Rosentrater KA (2008) No differences in decomposition rates observed between Bacillus thuringiensis and non-Bacillus thuringiensis corn residue incubated in the field. Agr J 100(1):163–168

    Article  Google Scholar 

  • Li X, Liu B, Cui J, Liu D, Ding S, Gilna B, Luo J, Fang Z, Cao W, Han Z (2011) No evidence of persistent effects of continuously planted transgenic insect-resistant cotton on soil microorganisms. Plant Soil 339(1–2):247–257

    Article  CAS  Google Scholar 

  • Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, Pennanen T et al (2013) Fungal community analysis by high-throughput sequencing of amplified markers—a user’s guide. New Phytol 2013; 199(1):288–299

    CAS  Google Scholar 

  • Liu W, Hao Lu H, Wu W, Kun Wei Q, Xu Chen Y, Thies JE (2008) Transgenic Bt rice does not affect enzyme activities and microbial composition in the rhizosphere during crop development. Soil Biol Biochem 40(2):475–486

    Article  CAS  Google Scholar 

  • Lu H, Wu W, Chen Y, Zhang X, Devare M, Thies JE (2010) Decomposition of Bt transgenic rice residues and response of soil microbial community in rapeseed–rice cropping system. Plant Soil 336(1–2):279–290

    Article  CAS  Google Scholar 

  • Madliger M, Sander M, Schwarzenbach RP (2010) Adsorption of transgenic insecticidal Cry1Ab protein to SiO2. 2. Patch-controlled electrostatic attraction. Environ Sci Technol 44(23):8877–8883

    Article  CAS  PubMed  Google Scholar 

  • Madliger M, Gasser CA, Sander M, Schwarzenbach RP (2011) Adsorption of transgenic insecticidal Cry1Ab protein to silica particles. Effects on transport and bioactivity. Environ Sci Technol 45:4377–4384

    Article  CAS  PubMed  Google Scholar 

  • Marchetti E, Accinelli C, Talame V, Epifani R (2007) Persistence of Cry toxins and cry genes from genetically modified plants in two agricultural soils. Agr Sus Dev 27(3):231–236

    Article  CAS  Google Scholar 

  • Mardis ER (2008) Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 9:387–402

    Article  CAS  PubMed  Google Scholar 

  • Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition on the rhizosphere. Soil Biol Biochem 33(11):1437–1445

    Article  CAS  Google Scholar 

  • Miethling-Graff R, Dockhorn S, Tebbe CC (2010) Release of recombinant Cry3b1 protein of Bt maize MON 88017 into field soil and detection of effects on the diversity of rhizosphere bacteria. Eur J Soil Biol 46:41–48

    Article  CAS  Google Scholar 

  • Muchaonyerwa P, Waladde S, Nyamugafata P, Mpepereki S, Ristori GG (2004) Persistence and impact on microorganisms of Bacillus thuringiensis proteins in some Zimbabwean soils. Plant Soil 266(1–2):41–46

    CAS  Google Scholar 

  • Muchaonyerwa P, Chevallier T, Pantani OL, Nyamugafata P, Mpepereki S, Chenu C (2006) Adsorption of the pesticidal toxin from Bacillus thuringiensis subsp tenebrionis on tropical soils and their particle-size fractions. Geoderma 133(3–4):244–257

    Article  CAS  Google Scholar 

  • Mungai NW, Motavalli PP, Nelson KA, Kremer RJ (2005) Differences in yields, residue composition and N mineralization dynamics of Bt and non-Bt-maize. Nutr Cycling Agroecosys 73(1):101–109

    Article  Google Scholar 

  • Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62(1):105–116

    Article  CAS  Google Scholar 

  • NRC (2010) Advancing the science of climate change. National Research Council. National Academies Press, Washington, DC, USA

    Google Scholar 

  • Oger P, Petit A, Dessaux Y (1997) Genetically engineered plants producing opines alter their biological environment. Nature 15:369–372

    CAS  Google Scholar 

  • Oliveira AP, Pampulha ME, Bennett JP (2008) A two-year field study with transgenic Bacillus thuringiensis maize: effects on soil microorganisms. Sci Tot Environ 405(1):351–357

    Article  CAS  Google Scholar 

  • Pagel-Wieder S, Niemeyer J, Fischer WR, Gessler F (2007) Effects of physical and chemical properties of soils on adsorption of the insecticidal protein (Cry1Ab) from Bacillus thuringiensis at Cry1Ab protein concentrations relevant for experimental field sites. Soil Biol Biochem 39(12):3034–3042

    Article  CAS  Google Scholar 

  • Pangrikar PP, Rokade PB, Gaikwad PD, Rupnar BD (2014) Impact of transgenic Bt cotton on functional fungal populations in rhizosphere soil. Int J Chem Environ Biol Sci 2(1):29–32

    Google Scholar 

  • Pauwels K, De Keersmaecker SCJ, De Schrijver A, du Jardin P, Roosens NHC, Herman P (2015) Next-generation sequencing as a tool for the molecular characterisation and risk assessment of genetically modified plants: added value or not? Trends Food Sci Technol 45:319–326

    Article  CAS  Google Scholar 

  • Pontiroli A, Simonet P, Frostegard A, Vogel TM, Monier JM (2007) Fate of transgenic plant DNA in the environment. Environ Biosafety Res 6(1–2):15–35

    Article  CAS  PubMed  Google Scholar 

  • Prischl M, Hackl E, Pastar M, Pfeiffer S, Sessitch A (2012) Genetically modified Bt maize lines containing cry3Bb1, cry1A105 or cry1Ab2 do not affect the structure and functioning of root-associated endophyte communities. Appl Soil Ecol 54:39–48

    Article  Google Scholar 

  • Rasche F, Velvis H, Zachow C, Berg G, van Elsas JD, Sessitsch A (2006) Impact of transgenic potatoes expressing anti-bacterial agents on bacterial endophytes is comparable with the effects of plant genotype, soil type and pathogen infection. J Appl Microbiol 43(3):555–565

    CAS  Google Scholar 

  • Ream JE, Sims SR, Leach JN (1994) Aerobic soil degradation of Bacillus thuringiensis var. kurstaki HD-73 protein bioactivity. Monsanto Company Laboratory Project MSL 13267, 1994; 11, Monsanto, St. Louis, MO

  • Rui YK, Yi GX, Zhao J, Wang BM, Li ZH, Zhai ZX, He ZP et al (2005) Changes of Bt toxin in the rhizosphere of transgenic Bt cotton and its influence on soil functional bacteria. W J Microbiol Biotechnol 21(6–7):1279–1284

    Article  CAS  Google Scholar 

  • Sander M, Madliger M, Schwarzenbach RP (2010) Adsorption of transgenic insecticidal Cry1Ab protein to SiO2. 1. Forces driving adsorption. Environ Sci Technol 44(1):8870–8876

    Article  CAS  PubMed  Google Scholar 

  • Sangwan RS, Tripathi S, Singh J, Narnoliya LK, Sangwan NS (2013) De novo sequencing and assembly of Centella asiatica leaf transcriptome for mapping of structural, functional and regulatory genes with special reference to secondary metabolism. Gene 525(1):58–76

    Article  CAS  PubMed  Google Scholar 

  • Sarkar B, Patra AK, Purakayastha TJ (2008) Transgenic Bt-cotton affects enzyme activity and nutrient availability in a sub-tropical Inceptisol. J Agron Crop Sci (4); 194: 289–296

  • Savka MA, Farrand SK (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotechnol 15:363–368

    Article  CAS  PubMed  Google Scholar 

  • Saxena D, Stotzky G (2001) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol Biochem 33:1225–1230

    Article  CAS  Google Scholar 

  • Saxena D, Stotzky G (2002) Bt toxin is not taken up from soil or hydroponic culture by corn, carrot, radish, or turnip. Plant Soil 239(2):165–172

    Article  CAS  Google Scholar 

  • Saxena D, Flores S, Stotzky G (2002) Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biol Biochem 34(1):133–137

    Article  CAS  Google Scholar 

  • Saxena D, Stewart CN, Altosaar I, Shu Q, Stotzky G (2004) Larvicidal Cry proteins from Bacillus thuringiensis are released in root exudates of transgenic B. thuringiensis corn, potato, and rice but not of B. thuringiensis canola, cotton, and tobacco. Plant Physiol Biochem 42(5):383–387

    Article  CAS  PubMed  Google Scholar 

  • Seres A, Kiss I, Nagy P, Sály P, Darvas B, Bakonyi G (2014) Arbuscular mycorrhizal fungi colonisation of Cry3 toxin-producing Bt maize and near isogenic maize. Plant Soil Environ 60(12):569–573

    CAS  Google Scholar 

  • Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 50(4):239–249

    Article  CAS  PubMed  Google Scholar 

  • Shen RF, Cai H, Gong WH (2006) Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil. Plant Soil 285(1–2):149–159

    Article  CAS  Google Scholar 

  • Shendure J, Ji H (2008) Next-generation DNA sequencing. Nature 26:1135–1145

    CAS  Google Scholar 

  • Sims SR, Holden LR (1996) Insect bioassay for determining soil degradation of Bacillus thuringiensis subsp. kurstaki Cry11A(b) protein in corn tissues. Environ Entomol 25:659–664

    Article  Google Scholar 

  • Sims SR, Ream JE (1997) Soil inactivation of the Bacillus thuringiensis subsp. kurstaki Cry IIA insecticidal protein within transgenic cotton tissue: laboratory microcosm and field studies. J Agricul Food Chem 45(4):1502–1505

    Article  CAS  Google Scholar 

  • Singer MJ, Munns DN (1999) Soils: an introduction. Prentice Hall, New Jersey

    Google Scholar 

  • Singh RJ, Ahlawat IPS, Singh S (2012) Effects of transgenic Bt cotton on soil fertility and biology under field conditions in sub-tropical Inseptisol. Environ Monit Ass 85(1):485–495

    Google Scholar 

  • Singh AK, Singh M, Dubey SK (2013a) Changes in Actinomycetes community structure under the influence of Bt transgenic brinjal crop in a tropical agroecosystem. BMC Microbiol 13:122–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh AK, Rai GK, Singh M, Dubey SK (2013b) Bacterial community structure in the rhizosphere of a Cry1Ac Bt-brinjal crop and comparison to its non-transgenic counterpart in the tropical soil. Microb Ecol 66(4):927–939

    Article  PubMed  Google Scholar 

  • Singh AK, Singh M, Dubey SK (2014) Rhizospheric fungal community structure of a Bt brinjal and a near isogenic variety. J Appl Microbiol 117(3):750–765

    Article  CAS  PubMed  Google Scholar 

  • Soni DK, Singh KM, Ghosh A, Chikara SK, Joshi CG, Dubey SK (2015) Whole-genome sequence of Listeria monocytogenes strains from clinical and environmental samples from Varanasi, India. Genome Announce 2015 3(1):e01496–14

    Google Scholar 

  • Stotzky G (2004) Persistence and biological activity in soil of the insecticidal proteins from Bacillus thuringiensis, especially from transgenic plants. Plant Soil 266(1–2):77–89

    CAS  Google Scholar 

  • Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun CX, Chen LJ, Wu ZJ, Zhou LK, Shimizu H (2007) Soil persistence of Bacillus thuringiensis (Bt) toxin from transgenic Bt cotton tissues and its effect on soil enzyme activities. Biol Fert Soils 43(5):617–620

    Article  Google Scholar 

  • Suryanarayanan TS, Venkatachalam A, Govinda Rajulu MB (2011) A comparison of endophyte assemblages in transgenic and non-transgenic cotton plant tissues. Curr Sci 101(11):1472–1474

    Google Scholar 

  • Tan F, Wang J, Feng Y, Chi G, Kong H, Qiu H, Wei S (2010) Bt corn plants and their straw have no apparent impact on soil microbial communities. Plant Soil 329(1–2):349–364

    Article  CAS  Google Scholar 

  • Tapp H, Stotzky G (1998) Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biol Biochem 30(4):471–476

    Article  CAS  Google Scholar 

  • Tarafdar JC, Rathore I, Shiva V (2012) Effect of transgenic cotton on soil biological health. Appl Biol Res 14(1):15–23

    Google Scholar 

  • Tarkalson DD, Kachman SD, Knops JMN, Thies JE, Wortmann CS (2008) Decomposition of Bt and non-Bt corn hybrid residues in the field. Nutr Cyc Agroecosys 80(3):211–222

    Article  CAS  Google Scholar 

  • Tomaszewski JE, Madliger M, Pedersen JA, Schwarzenbach RP, Sander M (2012) Adsorption of insecticidal Cry1Ab protein to humic substances. 2. Influence of humic and fulvic acid charge and polarity characteristics. Environ Sci Technol 46(18):9932–9940

    CAS  PubMed  Google Scholar 

  • Turrini A, Sbrana C, Giovannetti M (2015) Belowground environmental effects of transgenic crops: a soil microbial perspective. Res Microbiol 166:121–131

  • Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovannetti M (2004) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266(1–2):69–75

    CAS  Google Scholar 

  • Valverde JR, Marín S, Mellado RP (2014) Effect of herbicide combinations on Bt-maize rhizobacterial diversity. J Microbiol Biotechnol (24)11: 1473–483

  • Velmourougane K, Sahu A (2013) Impact of transgenic cottons expressing cry1Ac on soil biological attributes. Plant Soil Environ 59(3):108–114

    CAS  Google Scholar 

  • Verbruggen E, Kuramae EE, Hillekens R, de Hollander M, Kiers ET, Röling WFM, Kowalchuk GA (2012) Testing potential effects of maize expressing the Bacillus thuringiensis Cry1Ab endotoxin (Bt maize) on mycorrhizal fungal communities via DNA- and RNA-based pyrosequencing and molecular fingerprinting. Appl Environ Microbiol 78(20):7384–7392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197(4):1104–1109

    Article  PubMed  Google Scholar 

  • Wang H, Ye Q, Wang W, Wu L, Wu W (2006) Cry1Ab protein from Bt transgenic rice does not residue in rhizosphere soil. Environ Pol 143(3):449–455

    Article  CAS  Google Scholar 

  • Wei M, Tan F, Zhu H, Cheng K, Wu X, Wang J, Zhao K, Tang X (2012) Impact of Bt-transgenic rice (SHK601) on soil ecosystems in the rhizosphere during crop development. Plant Soil Environ 58(5):217–223

    CAS  Google Scholar 

  • WeiXiang W, Ye Q-f, Hang M, Xue-jun D, Wen-ming J (2004) Bt transgenic rice straw affects the culturable microbiota and dehydrogenase and phosphatase activities in a flooded paddy soil. Soil Biol Biochem 36(2):289–295

    Article  CAS  Google Scholar 

  • Wu WX, Liu W, Lu HH, Chen YX, Devare M, Thies J (2009) Use of C-13 labeling to assess carbon partitioning in transgenic and non-transgenic (parental) rice and their rhizosphere soil microbial communities. FEMS Microbiol Ecol 67(1):93–102

    Article  CAS  PubMed  Google Scholar 

  • Xue K, Luo HF, Qi HY, Zhang HX (2005) Changes in soil microbial community structure associated with two types of genetically engineered plants analyzing by PLFA. J Environ Sci 17(1):130–134

    CAS  Google Scholar 

  • Xue K, Serohijos RC, Devare M, Thies JE (2011) Decomposition rates and residue-colonizing microbial communities of Bacillus thuringiensis insecticidal protein Cry3Bb-expressing (Bt) and non-Bt corn hybrids in the field. Appl Environ Microbiol 77(3):839–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang W, Zhang M, Ding G (2012) Effect of transgenic Bt corn on bioactivities and nutrients in rhizosphere soil. Communi Soil Sci Plant Analysis 43(4):689–700

    Article  CAS  Google Scholar 

  • Yanni SF, Whalen JK, Simpson MJ, Janzen HH (2011) Plant lignin and nitrogen contents control carbon dioxide production and nitrogen mineralization in soils incubated with Bt and non-Bt corn residues. Soil Biol Biochem 43(1):63–69

    Article  CAS  Google Scholar 

  • Zhang YJ, Xie M, Peng DL (2014) Effects of the transgenic CrylAc and CpTI insect-resistant cotton SGK321 on rhizosphere soil microorganism populations in northern China. Plant Soil Environ 60(6):285–289

    CAS  Google Scholar 

  • Zhou XY, Huang QY, Cai P, Yu ZN (2007) Adsorption and insecticidal activity of toxin from Bacillus thuringiensis on rectorite. Pedosphere 17(4):513–521

    Article  CAS  Google Scholar 

  • Zurbrügg C, Hönemann L, Meissle M, Romeis J, Nentwig W (2010) Decomposition dynamics and structural plant components of genetically modified Bt maize leaves do not differ from leaves of conventional hybrids. Transgenic Res 19(2):257–267

    Article  PubMed  CAS  Google Scholar 

  • Zwahlen C, Hilbeck A, Gugerli P, Nentwig W (2003a) Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Mol Ecol12 (3): 765–775

  • Zwahlen C, Hilbeck A, Howald R, Nentwig W (2003b) Effects of transgenic Bt corn litter on the earthworm Lumbricus terrestris. Mol Ecol 12(4):1077–1086

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

One of the authors (AKS) was supported by CSIR-New Delhi, Government of India, in the form of JRF and SRF research fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suresh Kumar Dubey.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Handling Editor: Bhumi Nath Tripathi

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, A.K., Dubey, S.K. Current trends in Bt crops and their fate on associated microbial community dynamics: a review. Protoplasma 253, 663–681 (2016). https://doi.org/10.1007/s00709-015-0903-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-015-0903-5

Keywords

Navigation