Skip to main content
Log in

A Comparison of Soil Microbial Community Structure, Protozoa and Nematodes in Field Plots of Conventional and Genetically Modified Maize Expressing the Bacillus thuringiens is CryIAb Toxin

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Field trials were established at three European sites (Denmark, Eastern France, South-West France) of genetically modified maize (Zea mays L.) expressing the CryIAb Bacillus thuringiensis toxin (Bt), the near-isogenic non-Bt cultivar, another conventional maize cultivar and grass. Soil from Denmark was sampled at sowing (May) and harvest (October) over two years (2002, 2003); from E France at harvest 2002, sowing and harvest 2003; and from SW France at sowing and harvest 2003. Samples were analysed for microbial community structure (2003 samples only) by community-level physiological-profiling (CLPP) and phospholipid fatty acid analysis (PLFA), and protozoa and nematodes in all samples. Individual differences within a site resulted from: greater nematode numbers under grass than maize on three occasions; different nematode populations under the conventional maize cultivars once; and two occasions when there was a reduced protozoan population under Bt maize compared to non-Bt maize. Microbial community structure within the sites only varied with grass compared to maize, with one occurrence of CLPP varying between maize cultivars (Bt versus a conventional cultivar). An overall comparison of Bt versus non-Bt maize across all three sites only revealed differences for nematodes, with a smaller population under the Bt maize. Nematode community structure was different at each site and the Bt effect was not confined to specific nematode taxa. The effect of the Bt maize was small and within the normal variation expected in these agricultural systems.

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.

Similar content being viewed by others

References

  • J S Angle (1994) ArticleTitleRelease of transgenic plants: biodiversity and population-level considerations Mol. Ecol. 3 45–50

    Google Scholar 

  • C B Blackwood J S Buyer (2004) ArticleTitleSoil microbial communities associated with Bt and non-Bt corn in three soils J. Environ. Qual. 33 832–836 Occurrence Handle15224917 Occurrence Handle1:CAS:528:DC%2BD2cXksVyls7o%3D Occurrence Handle10.2134/jeq2004.0832

    Article  PubMed  CAS  Google Scholar 

  • K P Bottjer L W Bone S S Gill (1985) ArticleTitleNematoda: susceptibility of the eggs to Bacillus thuringiensis toxins Exp. Parasitol. 60 239–244 Occurrence Handle4029351 Occurrence Handle1:CAS:528:DyaL2MXlsFGrsr0%3D Occurrence Handle10.1016/0014-4894(85)90027-X

    Article  PubMed  CAS  Google Scholar 

  • M Bruinsma GA Kowalchuk JA Veen Particlevan (2002) Effects of Genetically Modified Plants on Soil Ecosystems Netherlands Institute of Ecology Heteren, Netherlands 63

    Google Scholar 

  • Bruinsma M A G Kowalchuk AJ Veen Particlevan (2003) ArticleTitleEffects of genetically modified plants on microbial communities and processes in soil Biol. Fertil. Soils 37 329–337

    Google Scholar 

  • J F Darbyshire R E Wheatley M P Greaves R H E Inkson (1974) ArticleTitleA rapid method for estimating bacterial and protozoan populations in soil Rev. Ecol. Biol. Sol 11 465–474

    Google Scholar 

  • K K Donegan C J Palm V J Fieland L A Porteous L M Ganio D L Schaller L Q Bucao R J Seidler (1995) ArticleTitleChanges in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var kurstaki endotoxin. Appl. Soil Ecol. 2 111–124

    Google Scholar 

  • K K Donegan D L Schaller J K Stone L M Ganio G Reed P B Hamm P J Seidler (1996) ArticleTitleMicrobial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var tenebrionis endotoxin. Transgenic Res. 5 25–35 Occurrence Handle1:CAS:528:DyaK28Xos1eltw%3D%3D

    CAS  Google Scholar 

  • L M Donnison G S Griffith J Hedger P J Hobbs R D Bardgett (2000) ArticleTitleManagement influences on soil microbial communities and their function in botanically diverse haymeadows of northern England and Wales Soil Biol. Biochem. 32 253–263 Occurrence Handle1:CAS:528:DC%2BD3cXhsVyhsrY%3D

    CAS  Google Scholar 

  • C F Drury J A Stone W I Findlay (1991) ArticleTitleMicrobial biomass and soil structure associated with corn, grasses and legumes Soil Sci. Soc. Am. J. 55 805–811 Occurrence Handle10.2136/sssaj1991.03615995005500030029x

    Article  Google Scholar 

  • N Escher B Kach W Nentwig (2000) ArticleTitleDecomposition of transgenic Bacillus thuringiensis maize by microorganisms and woodlice Basic Appl. Ecol. 1 161–169 Occurrence Handle10.1078/1439-1791-00024

    Article  Google Scholar 

  • A Frostegård A Tunlid E Bååth (1991) ArticleTitleMicrobial biomass measured as total lipid phosphate in soils of different organic content J. Microbiol. Methods 14 151–163

    Google Scholar 

  • S J Grayston S Wang C D Campbell A C Edwards (1998) ArticleTitleSelective influence of plant species on microbial diversity in the rhizosphere Soil Biol. Biochem. 30 369–378 Occurrence Handle1:CAS:528:DyaK1cXhvFWrsro%3D Occurrence Handle10.1016/S0038-0717(97)00124-7

    Article  CAS  Google Scholar 

  • B S Griffiths M Bonkowski G Dobson S Caul (1999) ArticleTitleChanges in the soil microbial community structure in the presence of microbial-feeding nematodes and protozoa Pedobiologia 43 297–304 Occurrence Handle1:CAS:528:DyaK1MXotFOhtLw%3D Occurrence Handle000083365500002

    CAS  ISI  Google Scholar 

  • B S Griffiths S Caul (1993) ArticleTitleMigration of bacterial-feeding nematodes, but not protozoa, to decomposing grass residues Biol. Fertil. Soils 15 201–207 Occurrence Handle10.1007/BF00361612

    Article  Google Scholar 

  • A T Groot M Dicke (2002) ArticleTitleInsect-resistant transgenic plants in a multi-trophic context Plant J. 31 387–406 Occurrence Handle12182699 Occurrence Handle1:CAS:528:DC%2BD38XnvVSqtrY%3D Occurrence Handle10.1046/j.1365-313X.2002.01366.x

    Article  PubMed  CAS  Google Scholar 

  • C A Hackett B S Griffiths (1997) ArticleTitleStatistical analysis of the time-course of Biolog substrate utilization J. Microbiol. Methods 30 63–69 Occurrence Handle1:CAS:528:DyaK2sXlslersLc%3D Occurrence Handle10.1016/S0167-7012(97)00045-6

    Article  CAS  Google Scholar 

  • T C J Hill E F McPherson J A Harris P Birch (1993) ArticleTitleMicrobial biomass estimated by phospholipids phosphate in soils with diverse microbial communities Soil Biol. Biochem. 25 1779–1786 Occurrence Handle10.1016/0038-0717(93)90183-C

    Article  Google Scholar 

  • D W Hopkins E G Gregorich (2003) ArticleTitleDetection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize Eur. J. Soil Sci. 54 793–800 Occurrence Handle10.1046/j.1351-0754.2003.0563.x

    Article  Google Scholar 

  • Höss S, Arndt M, Baumgarte S and Tebbe C C 2004 Effects of soil from experimental fields with transgenic corn on the nematode Caenorhabditis elegans. Abstract from Society of Environmental Toxicology and Chemistry, 14th Annual Meeting, Prague, April 2004.

  • M A Hurley M E Roscoe (1983) ArticleTitleAutomated statistical analysis of microbial enumeration by dilution series J. Appl. Bacteriol. 55 159–164

    Google Scholar 

  • James C 2003 Preview: global status of commercialized transgenic crops: 2003. ISAAA Briefs No.30. International Service for the Acquisition of Agri-biotech Applications, Ithaca, New York.

  • P C Jepson B A Croft G E Pratt (1994) ArticleTitleTest systems to determine the ecological risks posed by toxin release from Bacillus thuringiensis genes in crop plants Mol. Ecol. 3 81–89

    Google Scholar 

  • Manachini B, Fiore M C, Landi S and Arpaia S 2003 Nematode species assemblage in Bt-expressing transgenic eggplant and their isogenic control. In Biodiversity Implications of Genetically Modified Plants. Monte Verità, Ascona, Switzerland, Sept. 7–12, 2003. pp. 31–32.

  • B Manachini S Landi MC Fiore M Festa S Arpaia (2004) ArticleTitleFirst investigations on the effects of Bt-transgenic Brassica napus L on the trophic structure of the nematofauna IOBC wprs Bulletin 27 103–108

    Google Scholar 

  • J Meadows L W Bone (1990) ArticleTitleBacillus thuringiensis strains affect population growth of the free-living nematode Turbatrix aceti Invert. Reprod. Dev. 17 73–76

    Google Scholar 

  • P Nielsen S O Petersen (2000) ArticleTitleEster-linked polar lipid fatty acid profiles of soil microbial communities: a comparison of extraction methods and evaluation of interference from humic acids Soil Biol. Biochem 32 1241–1249 Occurrence Handle1:CAS:528:DC%2BD3cXlslyhs78%3D Occurrence Handle10.1016/S0038-0717(00)00041-9

    Article  CAS  Google Scholar 

  • F C Page (1976) ArticleTitleTaxonomic criteria for Limax amoebae with descriptions of three new species of Hartmanella and three of Vahlkampfia J. Protozool. 14 499–521

    Google Scholar 

  • RW Payne PW Lane PGN Digby SA Harding PK Leech GW Morgan AD Todd R Thompson G Tunnicliffe Wilson SJ Welhom RP White (1993) Genstat 5 Release Reference Manual Oxford University Press Oxford, UK

    Google Scholar 

  • D Saxena S Flores G Stotsky (2002) ArticleTitleBt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events Soil Biol. Biochem. 34 133–137 Occurrence Handle1:CAS:528:DC%2BD38XksVag

    CAS  Google Scholar 

  • D Saxena G Stotsky (2001) ArticleTitleBacillus 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 Occurrence Handle1:CAS:528:DC%2BD3MXlsV2js74%3D Occurrence Handle10.1016/S0038-0717(01)00027-X

    Article  CAS  Google Scholar 

  • A Schmalenberger C C Tebbe (2003) ArticleTitleGenetic profiling of noncultivated bacteria from the rhizospheres of sugar beet (Beta vulgaris) reveal field and annual variability but no effect of a transgenic herbicide resistance Can. J. Microbiol. 49 1–8 Occurrence Handle12674342 Occurrence Handle1:CAS:528:DC%2BD3sXitlSrurw%3D Occurrence Handle10.1139/w02-111

    Article  PubMed  CAS  Google Scholar 

  • M E Schutter J M Sandeno R P Dick (2001) ArticleTitleSeasonal, soil type and alternative management influences on microbial communities of vegetable cropping systems Biol. Fertil. Soils 34 397–410 Occurrence Handle1:CAS:528:DC%2BD3MXosFGntrg%3D

    CAS  Google Scholar 

  • SD Siciliano CM Theoret JR Freitas Particlede PJ Hucl JJ Germida (1998) ArticleTitleDifferences in the microbial communities associated with the roots of different cultivars of canola and wheat Can. J. Microbiol. 44 844–851 Occurrence Handle1:CAS:528:DyaK1cXnvFyksbg%3D Occurrence Handle10.1139/cjm-44-9-844

    Article  CAS  Google Scholar 

  • S R Sims J W Martin (1997) ArticleTitleEffect of the Bacillus thuringiensis insecticidal proteins CryIA(b), CryIA(c), CryIIA and CryIIIA on Folsomia candida and Xenylla grisea (Insecta: Collembola) Pedobiologia 41 412–416 Occurrence Handle1:CAS:528:DyaK2sXns1yntrw%3D Occurrence HandleA1997YA11200004

    CAS  ISI  Google Scholar 

  • S R Sims J E Ream (1997) ArticleTitleSoil inactivation of the Bacillus thuringiensis subsp kurstaki CryIIA insecticidal protein within transgenic cotton tissue: laboratory, microcosm and field studies. J. Agr. Food Chem. 45 1502–1505 Occurrence Handle1:CAS:528:DyaK2sXitVGhsro%3D

    CAS  Google Scholar 

  • J T Trevors P Kuikman B Watson (1994) ArticleTitleTransgenic plants and biogeochemical cycles Mol. Ecol. 3 57–64 Occurrence Handle1:CAS:528:DyaK2cXjtF2gsb8%3D

    CAS  Google Scholar 

  • R E Wheatley S Caul D Crabb T J Daniell B S Griffiths K Ritz (2003) ArticleTitleMicrobial population dynamics related to temporal variations in nitrification in three arable fields Eur. J. Soil Sci. 54 707–714 Occurrence Handle10.1046/j.1351-0754.2003.0558.x

    Article  Google Scholar 

  • W Wei-Xiang Y Qing-Fe M Hang (2004) ArticleTitleEffect of straws from Bt-transgenic rice on selected biological activities in water-flooded soil Eur. J. Soil Biol. 40 15–22

    Google Scholar 

  • F Widmer A Fließbach E Laczkó J Schulze-Aurich J Zeyer (2001) ArticleTitleAssessing soil biological characteristics: a comparison of bulk soil community DNA-, PLFA-, and BiologTM-analyses Soil Biol. Biochem. 33 1029–1036 Occurrence Handle1:CAS:528:DC%2BD3MXksVOrurY%3D Occurrence Handle10.1016/S0038-0717(01)00006-2

    Article  CAS  Google Scholar 

  • J E Wilkinson D Twell K Lindsey (1997) ArticleTitleActivities of CaMV 35S and nos promoters in pollen: implications for field release of transgenic plants J. Exp. Bot. 48 265–275 Occurrence Handle1:CAS:528:DyaK2sXhvFSitrw%3D

    CAS  Google Scholar 

  • L L Wolfenbarger P R Phifer (2000) ArticleTitleThe ecological risks and benefits of genetically engineered plants Science 290 2088–2093 Occurrence Handle11118136 Occurrence Handle1:CAS:528:DC%2BD3cXptVyjtL8%3D Occurrence Handle000165870600039 Occurrence Handle10.1126/science.290.5499.2088

    Article  PubMed  CAS  ISI  Google Scholar 

  • W-X Wu Q-F Ye H Min X-J Duan W-M Jin (2004) ArticleTitleBt-transgenic rice straw affects the culturable microbiota and dehydrogenase and phosphatase activities in a flooded paddy soil Soil Biol. Biochem. 36 289–295 Occurrence Handle1:CAS:528:DC%2BD2cXmvFGrtw%3D%3D

    CAS  Google Scholar 

  • L Yu R E Berry B A Croft (1997) ArticleTitleEffects of Bacillus thuringiensis toxin in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nites (Acari: Oribatidae) J. Econ. Entomol. 90 113–118

    Google Scholar 

  • L Zelles Q Y Bai R X Ma R Rackwitz K Winter F Beese (1994) ArticleTitleMicrobial biomass, metabolic activity and nutritional status determined from fatty acid patterns and poly-hydroxybutyrate in agriculturally managed soils Soil Biol. Biochem. 26 439–446 Occurrence Handle1:CAS:528:DyaK2cXisVehu7Y%3D Occurrence Handle10.1016/0038-0717(94)90175-9

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B.S. Griffiths.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Griffiths, B., Caul, S., Thompson, J. et al. A Comparison of Soil Microbial Community Structure, Protozoa and Nematodes in Field Plots of Conventional and Genetically Modified Maize Expressing the Bacillus thuringiens is CryIAb Toxin. Plant Soil 275, 135–146 (2005). https://doi.org/10.1007/s11104-005-1093-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-005-1093-2

Keywords

Navigation