Skip to main content

Effects of conventionally bred and Bacillus thuringiensis (Bt) maize varieties on soil microbial biomass and activity

Abstract

Genetically modified (GM) maize containing genes from the soil bacterium Bacillus thuringiensis (Bt) was cultivated on 29% of the total maize production area worldwide in 2009. Most studies to date compare Bt-maize varieties with their near isogenic lines; however, there is little information on the variability of conventional maize breeding lines and how the effects of Bt varieties are ranked within. In our study on the potential risks of Bt-maize varieties, we analyzed tissue quality and compared the effects of ten conventional and GM maize varieties on soil microbiological properties in a replicated climate chamber experiment. All maize varieties were cultivated twice in the same soil microcosm. Shoot yields and soluble C in leaf tissue of Bt varieties were higher than the ones of non-Bt. Soil dehydrogenase activity was reduced by 5% under Bt varieties compared to non-Bt, while most of the other soil microbial properties (soil microbial biomass, basal respiration) showed no significant differences between Bt and non-Bt varieties. The leaves and roots of one Bt variety were decomposed to a greater extent than the ones of its near isogenic line; the conventional breeding lines also showed higher values. Changes in crop and soil parameters were found when comparing the first and the second crops, but the effects of repeated cropping were the same for all tested varieties. For the studied parameters, the variation among non-Bt-maize varieties was similar to the difference between Bt and non-Bt varieties.

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

Fig. 1
Fig. 2

References

  1. Anderson TH, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25:393–395

    Article  Google Scholar 

  2. Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecol Lett 9:196–214

    PubMed  Article  CAS  Google Scholar 

  3. Bartsch D, Devos Y, Hails R, Kiss J, Krogh PH, Mestdagh S, Nuti M, Sessitsch A, Sweet J, Gathmann A (2010) Environmental impact of genetically modified maize expressing Cry1 proteins. In: Kempken F, Jung C (eds) Genetic modification of plants, vol 64. Biotechnology in agriculture and forestry. Springer, Berlin, pp 575–614

    Google Scholar 

  4. 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 14:2539–2551

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  6. Broer I, Schiemann J (2009) Thesenpapier: Biologische Sicherheitsforschung an gentechnisch veränderten Pflanzen. Gesellschaft für Pflanzenbiotechnologie, p 6

  7. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  8. Castaldini M, Turrini A, Sbrana C, Benedetti A, Marchionni M, Mocali S, Fabiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovannetti M (2005) Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 71:6719–6729

    PubMed  Article  CAS  Google Scholar 

  9. Clark BW, Phillips TA, Coats JR (2005) Environmental fate and effects of Bacillus thuringiensis (Bt) proteins from transgenic crops: a review. J Agr Food Chem 53:4643–4653

    Article  CAS  Google Scholar 

  10. 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 33:837–843

    PubMed  Article  CAS  Google Scholar 

  11. Devare M, Londoño-R LM, Thies JE (2007) Neither transgenic Bt maize (MON863) nor tefluthrin insecticide adversely affect soil microbial activity or biomass: a 3-year field analysis. Soil Biol Biochem 39:2038–2047

    Article  CAS  Google Scholar 

  12. Dierauer HU, Böhler K (2008) Bio-Maissortenversuch 2007. Forschungsinstitut für Biologischen Landbau, Frick, p 8

    Google Scholar 

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

    Article  Google Scholar 

  14. Escher N, Käch B, Nentwig W (2000) Decomposition of transgenic Bacillus thuringiensis-maize by microorganisms and woodlice Porcellio scaber (Crustacea: Isopoda). Basic Appl Ecol 1:161–169

    Article  Google Scholar 

  15. FAL, FAW, RAC (1996) Referenzmethoden der Eidg. landwirtschaftlichen Forschungsanstalten - 1. Bodenuntersuchung zur Düngeberatung. Zürich-Reckenholz

  16. FAO (2011) Available at http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor. Accessed 21 April 2011

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

    Article  CAS  Google Scholar 

  18. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  19. GMO Compass (2011) Available at http://www.gmo-compass.org/eng/agri_biotechnology/gmo_planting/341.genetically_modified_maize_global_area_under_cultivation.html. Accessed 21 April 2011

  20. Griffiths BS, Caul S, Thompson J, Birch ANE, Scrimgeour C, Andersen MN, Cortet J, Messèan A, Sausse C, Lacroix B, Krogh PH (2005) A comparison of soil microbial community structure, protozoa and nematodes in field plots of conventional and genetically modified maize expressing the Bacillus thuringiensis Cry1Ab toxin. Plant Soil 275:135–146

    Article  CAS  Google Scholar 

  21. Griffiths BS, Heckmann L-H, Caul S, Thompson J, Scrimgeour C, Krogh PH (2007) Varietal effects of eight paired lines of transgenic Bt maize and near-isogenic non-Bt maize on soil microbial and nematode community structure. Plant Biotech J 5:60–68

    Article  CAS  Google Scholar 

  22. Griffiths B, Caul S, Thompson J, Hackett C, Cortet J, Pernin C, Krogh P (2008) Soil microbial and faunal responses to herbicide tolerant maize and herbicide in two soils. Plant Soil 308:93–103

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Icoz I, Saxena D, Andow DA, 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

    PubMed  Article  CAS  Google Scholar 

  26. JMP (2008) JMP 8.0 statistical discovery. SAS Institute Inc., Cary

  27. Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem 28:25–31

    Article  CAS  Google Scholar 

  28. Joergensen RG, Mueller T (1996) The fumigation extraction method to estimate soil microbial biomass: calibration of the kEN-factor. Soil Biol Biochem 28:33–37

    Article  CAS  Google Scholar 

  29. Kravchenko A, Hao X, Robertson G (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 

  30. Lang A, Arndt M, Beck R, Bauchhenß J (2005) Monitoring der Umweltwirkungen des Bt-Gens. Schriftenreihe der Bayerischen Landesanstalt für Landwirtschaft. Freising-Weihenstephan

  31. 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. Agron J 100:163–168

    Article  Google Scholar 

  32. Leinweber P, Schulten HR, Körschens M (1995) Hot water extracted organic matter: chemical composition and temporal variations in a long term field experiment. Biol Fertil Soils 10:17–23

    Article  Google Scholar 

  33. Mäder P, Fließbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697

    PubMed  Article  Google Scholar 

  34. Manachini B, Lozzia GC (2002) First investigations into the effects of Bt corn crop on Nematofauna. Bollettino di Zoologia Agraria e di Bachicoltura 34:85–96

    Google Scholar 

  35. Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 316:1475–1477

    PubMed  Article  CAS  Google Scholar 

  36. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160

    Article  Google Scholar 

  37. Poerschmann J, Gathmann A, Augustin J, Langer U, Gorecki T (2005) Molecular composition of leaves and stems of genetically modified Bt and near-isogenic non-Bt maize—characterization of lignin patterns. J Environ Qual 34:1508–1518

    PubMed  Article  CAS  Google Scholar 

  38. Raubuch M, Roose K, Warnstorff K, Wichern F, Joergensen RG (2007) Respiration pattern and microbial use of field-grown transgenic Bt-maize residues. Soil Biol Biochem 39:2380–2389

    Article  CAS  Google Scholar 

  39. Raubuch M, Behr K, Roose K, Joergensen RG (2010) Specific respiration rates, adenylates, and energy budgets of soil microorganisms after addition of transgenic Bt-maize straw. Pedobiologia 53:191–196

    Article  CAS  Google Scholar 

  40. Sanvido O, Stark M, Romeis J, Bigler F (eds) (2006) Ecological impacts of genetically modified crops, vol 1. ART-Schriftenreihe. Agroscope Reckenholz-Tänikon Research Station, Zürich

    Google Scholar 

  41. Saxena D, Stotzky G (2001a) 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 

  42. Saxena D, Stotzky G (2001b) Bt corn has a higher lignin content than non-Bt corn. Am J Bot 88:1704–1706

    PubMed  Article  CAS  Google Scholar 

  43. Saxena D, Flores S, Stotzky G (1999) Insecticidal toxin in root exudates from Bt-corn. Nature 402:480

    PubMed  CAS  Google Scholar 

  44. 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 42:383–387

    PubMed  Article  CAS  Google Scholar 

  45. Sims S, Martin J (1997) Effect 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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  47. Tabashnik B, Carrière Y, Dennehy TJ, Morin S, Sisteron MS, Roush RT, Shelton AM, Zhao J-Z (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J Econ Entomol 96:1031–1038

    PubMed  Article  CAS  Google Scholar 

  48. Tabashnik BE, Gassmann AJ, Crowder DW, Carriere Y (2008) Insect resistance to Bt crops: evidence versus theory. Nature Biotech 26:199–202

    Article  CAS  Google Scholar 

  49. Tabashnik BE, Van Rensburg JBJ, Carrière Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102:2011–2025

    PubMed  Article  CAS  Google Scholar 

  50. Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Chemical and microbiological properties, vol 9. Agronomy monograph, 2nd edn. American Society of Agronomy & Soil Science Society of America, Madison, pp 903–947

    Google Scholar 

  51. Tapp H, Stotzky G (1995) Insecticidal activity of the toxins Bacillus thuringiensis subspecies kurstaki and tenebrionis in soil. Appl Environ Microbiol 61:1786–1790

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  53. Tarkalson DD, Kachman ED, Knops JMN, Thies JE, Wortmann CS (2008) Decomposition of Bt and non-Bt corn hybrid residues in the field. Nutr Cycl Agroecosyst 80:211–222

    Article  CAS  Google Scholar 

  54. Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovannetti M (2005) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266:69–75

    Article  Google Scholar 

  55. Van Rensburg JBJ (2007) First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S Afr J Plant Soil 24:147–151

    Google Scholar 

  56. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  57. Wei Xiang W, Qing-fu Y, Hang M, Xue-jun D, Wen-ming J (2004a) Bt-transgenic rice straw affects the culturable microbiota and dehydrogenase and phosphatase activities in a flooded paddy soil. Soil Biol Biochem 36:289–295

    Article  Google Scholar 

  58. Wei Xiang W, Qing Fu Y, Hang M (2004b) Effect of straws from Bt-transgenic rice on selected biological activities in water-flooded soil. Eur J Soil Biol 40:15–22

    Article  Google Scholar 

  59. Yu L, Berry R, Croft B (1997) Effects of Bacillus thuringiensis toxins in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Oribatidae). J Econ Entomol 90:113–118

    Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

The work of Kathi Hothum and Antje Stotz as part of their practical stage at FiBL is gratefully acknowledged. We are especially grateful to Prof. Dr. Geneviève Défago (ETH, Zürich) who kindly provided the seeds of genetically modified Bt-maize that we were otherwise not able to achieve. The project was funded by the Swiss National Science Foundation in the frame of the NFP59 “Benefits and Risks of the Deliberate Release of Genetically Modified Plants.” Within the framework of NFP59, we thank Michael Sander and Michael Madliger (both ETH, Zürich) for their support in the quantification of the Cry1Ab proteins and Claudia Zwahlen (Uni Neuchâtel) for the helpful comments on the outcome of this project. Two unknown reviewers provided valuable input to the submitted manuscript and are gratefully acknowledged here.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Andreas Fließbach.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fließbach, A., Messmer, M., Nietlispach, B. et al. Effects of conventionally bred and Bacillus thuringiensis (Bt) maize varieties on soil microbial biomass and activity. Biol Fertil Soils 48, 315–324 (2012). https://doi.org/10.1007/s00374-011-0625-6

Download citation

Keywords

  • Bt-maize
  • Soil fertility
  • Cry1Ab
  • GMO
  • Microbial biomass
  • Soil respiration
  • Dehydrogenase
  • Mycorrhiza