Skip to main content
SpringerLink
Log in

Effects of genetically modified plants on microbial communities and processes in soil

  • Review Article
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The development and use of genetically modified plants (GMPs) has been a topic of considerable public debate in recent years. GMPs hold great promise for improving agricultural output, but the potential for unwanted effects of GMP use is still not fully understood. The majority of studies addressing potential risks of GMP cultivation have addressed only aboveground effects. However, recent methodological advances in soil microbial ecology have allowed research focus to move underground to try to gain knowledge of GMP-driven effects on the microbial communities and processes in soil that are essential to key terrestrial ecosystem functions. This review gives an overview of the research performed to date on this timely topic, highlighting a number of case studies. Although such research has advanced our understanding of this topic, a number of knowledge gaps still prevent full interpretation of results, as highlighted by the failure of most studies to assign a definitively negative, positive or neutral effect to GMP introduction. Based upon our accumulating, yet incomplete, understanding of soil microbes and processes, we propose a synthesis for the case-by-case study of GMP effects, incorporating assessment of the potential plant/ecosystem interactions, accessible and relevant indicators, and tests for unforeseen effects.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahrenholtz I, Harms K, De Vries J, Wackernagel W (2000) Increased killing of Bacillus subtilis on the hair roots of transgenic T4 lysozyme-producing potatoes. Appl Environ Microbiol 66:1862–1865

    CAS  PubMed  Google Scholar 

  • Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) (1995) Molecular microbial ecology manual. Kluwer, Dordrecht

  • Amann R, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  Google Scholar 

  • Atlas RM, Bartha R (1998) Microbial ecology: fundamentals and applications, 4th edn. Benjamin/Cummings Science, San Francisco, Calif., pp 99–140, 332–459

    Google Scholar 

  • Berg P, Baltimore D, Boyer HW, Cohen SN, Davis RW, Hogness DS, Nathans D, Roblin R, Watson JD, Weissman S, Zinder ND (1974) Letter: potential biohazards of recombinant DNA molecules. Science 185:303

    CAS  Google Scholar 

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Google Scholar 

  • Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73:S1377–S1383

    Google Scholar 

  • Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14:695–700

    CAS  PubMed  Google Scholar 

  • Broglie K, Chet I, Holliday M, Cressmann R, Biddle P, Knowlton S, Mauvais CJ, Broglie R (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254:1194–1197

    CAS  Google Scholar 

  • Bruinsma M, Kowalchuk GA, Van Veen JA (2002) Effects of genetically modified plants on soil ecosystems. Ponsen and Looijen, Wageningen

  • Ceccherini MT, Poté J, Kay E, Van VT, Maréchal J, Pietramellara G, Nannipieri P, Vogel TM, Simonet P (2003) Degradation and transformability of DNA from transgenic leaves. Appl Environ Microbiol 69:673–678

    Article  CAS  PubMed  Google Scholar 

  • Clausen M, Kräuten R, Schachermayr G, Potrykus I, Sautter C (2000) Antifungal activity of a virally encoded gene in transgenic wheat. Nature Biotech 18:446–449

    Article  CAS  Google Scholar 

  • Cohen S, Chang A, Boyer H, Helling R (1973) Construction of biologically functional bacterial plasmids in vitro. Proc Natl Acad Sci USA 70:3240–3244

    CAS  PubMed  Google Scholar 

  • Cowgill SE, Bardgett RD, Kiezebrink DT, Atkinson HJ (2002) The effect of transgenic nematode resistance on non-target organisms in the potato rhizosphere. J Appl Ecol 39:915–923

    Article  Google Scholar 

  • Di Giovanni GD, Watrud LS, Seidler RJ, Widmer F (1999) Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using biolog GN metabolic fingerprinting and enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Microb Ecol 37:129–139

    Article  PubMed  Google Scholar 

  • 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 

  • Donegan KK, Schaller 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. Transgenic Res 5:25–35

    CAS  Google Scholar 

  • Donegan KK, Seidler RJ, Doyle JD, Porteous LA, Digiovanni G, Widmer F, Watrud LS (1999) A field study with genetically engineered alfalfa inoculated with recombinant Sinorhizobium meliloti: effects on the soil ecosystem. J Appl Ecol 36:920–936

    Article  Google Scholar 

  • Donegan KK, Seidler RJ, Fieland VJ, Schaller DL, Palm CJ, Ganio LM, Cardwell DM, Steinberger Y (1997) Decomposition of genetically engineered tobacco under field conditions: persistence of the proteinase inhibitor I product and effects on soil microbial respiration and protozoa, nematode and microarthropod populations. J Appl Ecol 34:767–777

    Google Scholar 

  • Dunfield KE, Germida JJ (2001) Diversity of bacterial communities in the rhizosphere and root interior of field-grown genetically modified Brassica napus. FEMS Microbiol Ecol 82:1–9

    Article  Google Scholar 

  • Düring K, Porsch P, Fladung M, Lorz H (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Ewinia carotovora. Plant J 3:587–598

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Focht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Adv Microb Ecol 1:135–214

    CAS  Google Scholar 

  • Gebhard F, Smalla K (1999) Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer. FEMS Microbiol Ecol 28:261–272

    Article  CAS  Google Scholar 

  • Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1999) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153

    Article  CAS  Google Scholar 

  • Griffiths BS, Geoghegan IE, Robertson WM (2000) Testing genetically engineered potato, producing the lectins GNA and Con A, on non-target soil organisms and processes. J Appl Ecol 37:159–170

    Article  Google Scholar 

  • Gyamfi S, Pfeifer U, Stierschneider M, Sessitsch A (2002) Effects of transgenic glufosinate-tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. FEMS Microbiol Ecol 41:181–190

    Article  CAS  Google Scholar 

  • Head IM, Saunders JR, Pickup RW (1998) Microbial evolution, diversity and ecology: a decade of ribosomal RNA analysis of uncultured microorganisms. Microb Ecol 35:1–21

    PubMed  Google Scholar 

  • Heuer H, Smalla K (1999) Bacterial phyllosphere communities of Solanum tuberosum L. and T4-lysozyme-producing transgenic variants. FEMS Microbiol Ecol 28:357–371

    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 68:1325–1335

    Article  CAS  PubMed  Google Scholar 

  • Hooper AB (1990) Biochemistry of the nitrifying litho-autotrophic bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Springer, Berlin Heidelberg New York, pp 239–265

  • Hopkins DW, Webster EA, Chudek JA, Halpin C (2001) Decomposition in soil of tobacco plants with genetic modifications to lignin biosynthesis. Soil Biol Biochem 33:1455–1462

    Article  CAS  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Ann Rev Microbiol 55:485–529

    Article  CAS  Google Scholar 

  • Kowalchuk GA, de Souza FA, Van Veen JA (2002) Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol Ecol 11:571–581

    Article  CAS  PubMed  Google Scholar 

  • Kowalski SP, Ebora RV, Kryder RD, Potter RH (2002) Transgenic crops, biotechnology and ownership rights: what scientists need to know. Plant J 31:407–421

    Article  CAS  PubMed  Google Scholar 

  • Lottmann J, Berg G (2001) Phenotypic and genotypic characterisation of antagonistic bacteria associated with roots of transgenic and non-transgenic potato plants. Microbiol Res 156:75–82

    CAS  PubMed  Google Scholar 

  • Lottmann J, Heuer H, Smalla K, Berg G (1999) Influence of transgenic T4-lysozyme-producing potato plants on potentially beneficial plant-associated bacteria. FEMS Microbiol Ecol 29:365–377

    Article  CAS  Google Scholar 

  • Lottmann J, Heuer H, De Vries J, Mahn A, Düring K, Wackernagel W, Smalla K, Berg G (2000) Establishment of introduced antagonistic bacteria in the rhizosphere of transgenic potatoes and their effect on the bacterial community. FEMS Microbiol Ecol 33:41–49

    Article  PubMed  Google Scholar 

  • Lukow T, Dunfield PF, Liesack W (2000) Use of T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiol Ecol 32:241–247

    Article  CAS  PubMed  Google Scholar 

  • Lusso M, Kuc J (1996) The effect of sense and antisense expression of the PR-N gene for β-1,3,-glucanase on disease resistance of tobacco to fungi and viruses. Plant Pathol 49:267–283

    Article  CAS  Google Scholar 

  • Maddaloni M, Forlani F, Balmas V, Donini G, Stasse L, Corazza L, Motto M (1997) Tolerance to the fungal pathogen Rhizoctonia solani AG4 of transgenic tobacco expressing the maize ribosome-inactivating protein b-32. Transgenic Res 6:393–402

    CAS  Google Scholar 

  • Mansouri H, Petit A, Oger P, Dessaux Y (2002) Engineered rhizosphere: the trophic bias generated by opine-producing plants is independent of the opine type, the soil origin and the plant species. Appl Environ Microbiol 68:2562–2566

    Article  CAS  PubMed  Google Scholar 

  • Masoud SA (1996) Constitutive expression of an inducible β-1,3-glucanase in alfalfa reduces disease severity caused by the oomycete pathogen Phytophthora megasperma f. sp medicaginis, but does not reduce disease severity of chitin-containing fungi. Transgenic Res 5:313–323

    CAS  Google Scholar 

  • Murray F, Llewellyn D, McFadden H, Last D, Dennis ES, Peacock WJ (1999) Expression of the Talaromyces flavus glucose oxidase gene in cotton and tobacco reduces fungal infection, but is also phytotoxic. Mol Breed 5:219–232

    Article  CAS  Google Scholar 

  • Neuhaus JM, Flores S, Keefe D, Ahl-Goy P, Meins F Jr (1992) The function of vacuolar ß-1,3,-glucanase investigated by antisense transformation. Susceptibility of transgenic Nicotiana sylvestris plants to Cercospora nicotianae infection. Plant Mol Biol 19:803–813

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Oger P, Mansouri H, Dessaux Y (2000) Effect of crop rotation and soil cover on alteration of the soil microflora generated by the culture of transgenic plants producing opines. Mol Ecol 9:881–890

    Article  CAS  PubMed  Google Scholar 

  • Palm CJ, Donegan KK, Harris D, Seidler RJ (1994) Quantification in soil of Bacillus thuringiensis var. kurstaki δ-endotoxin from transgenic plants. Mol Ecol 3:145–151

    CAS  Google Scholar 

  • Pankhurst CE, Doube BM, Gupta VVSR (1997) Biological indicators of soil health. CAB International, Wallingford

  • 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 

  • Schmalenberger A, Tebbe CC (2002) Bacterial community composition in the rhizosphere of a transgenic, herbicide-resistant maize (Zea mays) and comparison to its non-transgenic cultivar Bosphore. FEMS Microbiol Ecol 40:29–37

    CAS  Google Scholar 

  • Serageldin I (1999) Biotechnology and food security in the 21st century. Science 285:387–389

    Article  CAS  PubMed  Google Scholar 

  • Siciliano SD, Germida JJ (1999) Taxonomic diversity of bacteria associated with the roots of field-grown transgenic Brassica napus cv Quest, compared to the non-transgenic B. napus cv. Excel and B. rapa cv. Parkland. FEMS Microbiol Ecol 29:263–272

    Article  CAS  Google Scholar 

  • Siciliano SD, Theoret CM, De Freitas JR, Hucl PJ, Germida JJ (1998) Differences in the microbial communities associated with the roots of different cultivars of canola and wheat. Can J Microbiol 44:844–851

    Article  CAS  Google Scholar 

  • Stephen JR, Kowalchuk GA (2002) Ribotyping methods for assessment of in situ microbial community structure. In: Bitton G (ed) Encyclopedia of environmental microbiology, vol 5. Wiley, New York, pp 2728–2741

  • Tahiri-Alaoui A, Grison R, Gianinazzi-Pearson V, Toppan A, Gianinazzi S (1994) The impact of the constitutive expression of chitinases in roots of transgenic tobacco on arbuscular mycorrhizal fungi. Abstract 406 of the 7th international symposium on molecular plant-microbe interactions, Edinburgh, 26 June–1 July, 1994

  • Tsaftaris AS, Polidoris AN, Karavangeli M, Nianiou-Obeidat I, Madesis P, Goudoula C (2000) Transgenic crops: recent developments and prospects. In: Balazs E, Galante E, Lynch JM, Schepers JS, Toutant JP, Werner D, Werry PATJ (eds) Biological resource management. Springer, Berlin Heidelberg New York, pp 187–203

  • Van der Putten WH, Peters BAM (1997) How soil-borne pathogens may affect plant communities. Ecology 78:1785–1795

    Google Scholar 

  • Vierheilig H, Alt M, Neuhaus J, Boller T, Wiemken A (1993) Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mosseae. Mol Plant Microbe Interact 6:261–264

    CAS  Google Scholar 

  • Vierheilig H, Alt M, Lange J, Gut-Rella M, Wiemken A, Boller T (1995) Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 61:3031–3034

    CAS  Google Scholar 

Download references

Acknowledgements

This work was sponsored by the Dutch Ministry of Housing, Spatial Planning and the Environment (VROM), and advised by the State Committee on Genetic Modification (COGEM). We thank W.A. Brandenburg (Plant Research International), R.G. van der Graaf (VROM), D.C.M. Glandorf (RIVM/CSR/Bureau GGO), J.D. van Elsas (Plant Research International) and H.J. Laanbroek (NIOO-KNAW Center for Limnology) for their input and advice, and W. de Boer for critical reading of the manuscript. This is publication no. XXXX of the Netherlands Institute of Ecology (NIOO-KNAW).

Author information

Authors and Affiliations

  1. Netherlands Institute of Ecology (NIOO-KNAW), Center for Terrestrial Ecology (CTE), Boterhoeksestraat 48, P.O. Box 40, 6666 ZG, Heteren, The Netherlands

    M. Bruinsma, G. A. Kowalchuk & J. A. van Veen

Authors
  1. M. Bruinsma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. A. Kowalchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. A. van Veen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. A. van Veen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bruinsma, M., Kowalchuk, G.A. & van Veen, J.A. Effects of genetically modified plants on microbial communities and processes in soil. Biol Fertil Soils 37, 329–337 (2003). https://doi.org/10.1007/s00374-003-0613-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-003-0613-6

Keywords

Search

Navigation