Biology and Fertility of Soils

, Volume 37, Issue 6, pp 329–337 | Cite as

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

  • M. Bruinsma
  • G. A. Kowalchuk
  • J. A. van VeenEmail author
Review Article


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.


Genetically modified plants Soil microbial communities Soil microbial processes Risk assessment 



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).


  1. 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 66:1862–1865PubMedGoogle Scholar
  2. Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) (1995) Molecular microbial ecology manual. Kluwer, DordrechtGoogle Scholar
  3. Amann R, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual cells without cultivation. Microbiol Rev 59:143–169PubMedGoogle Scholar
  4. Atlas RM, Bartha R (1998) Microbial ecology: fundamentals and applications, 4th edn. Benjamin/Cummings Science, San Francisco, Calif., pp 99–140, 332–459Google Scholar
  5. 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 185:303Google Scholar
  6. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573Google Scholar
  7. Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73:S1377–S1383Google Scholar
  8. 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 14:695–700PubMedGoogle Scholar
  9. 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 254:1194–1197Google Scholar
  10. Bruinsma M, Kowalchuk GA, Van Veen JA (2002) Effects of genetically modified plants on soil ecosystems. Ponsen and Looijen, WageningenGoogle Scholar
  11. 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 69:673–678CrossRefPubMedGoogle Scholar
  12. Clausen M, Kräuten R, Schachermayr G, Potrykus I, Sautter C (2000) Antifungal activity of a virally encoded gene in transgenic wheat. Nature Biotech 18:446–449CrossRefGoogle Scholar
  13. Cohen S, Chang A, Boyer H, Helling R (1973) Construction of biologically functional bacterial plasmids in vitro. Proc Natl Acad Sci USA 70:3240–3244PubMedGoogle Scholar
  14. 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 39:915–923CrossRefGoogle Scholar
  15. 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 37:129–139CrossRefPubMedGoogle Scholar
  16. 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 2:111–124CrossRefGoogle Scholar
  17. 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 5:25–35Google Scholar
  18. 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 36:920–936CrossRefGoogle Scholar
  19. 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 34:767–777Google Scholar
  20. 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 82:1–9CrossRefGoogle Scholar
  21. Düring K, Porsch P, Fladung M, Lorz H (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Ewinia carotovora. Plant J 3:587–598CrossRefGoogle Scholar
  22. Escher N, Käch B, Nentwig W (2000) Decomposition of transgenic Bacillus thuringiensis maize by microorganisms and woodlice Porcellio scaber (Crustacea: Isopoda). Basic Appl Ecol 1:161–169Google Scholar
  23. Focht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Adv Microb Ecol 1:135–214Google Scholar
  24. 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 28:261–272CrossRefGoogle Scholar
  25. Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1999) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153CrossRefGoogle Scholar
  26. 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 37:159–170CrossRefGoogle Scholar
  27. 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 41:181–190CrossRefGoogle Scholar
  28. Head IM, Saunders JR, Pickup RW (1998) Microbial evolution, diversity and ecology: a decade of ribosomal RNA analysis of uncultured microorganisms. Microb Ecol 35:1–21PubMedGoogle Scholar
  29. Heuer H, Smalla K (1999) Bacterial phyllosphere communities of Solanum tuberosum L. and T4-lysozyme-producing transgenic variants. FEMS Microbiol Ecol 28:357–371CrossRefGoogle Scholar
  30. 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 68:1325–1335CrossRefPubMedGoogle Scholar
  31. Hooper AB (1990) Biochemistry of the nitrifying litho-autotrophic bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Springer, Berlin Heidelberg New York, pp 239–265Google Scholar
  32. Hopkins DW, Webster EA, Chudek JA, Halpin C (2001) Decomposition in soil of tobacco plants with genetic modifications to lignin biosynthesis. Soil Biol Biochem 33:1455–1462CrossRefGoogle Scholar
  33. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Ann Rev Microbiol 55:485–529CrossRefGoogle Scholar
  34. 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 11:571–581CrossRefPubMedGoogle Scholar
  35. Kowalski SP, Ebora RV, Kryder RD, Potter RH (2002) Transgenic crops, biotechnology and ownership rights: what scientists need to know. Plant J 31:407–421CrossRefPubMedGoogle Scholar
  36. Lottmann J, Berg G (2001) Phenotypic and genotypic characterisation of antagonistic bacteria associated with roots of transgenic and non-transgenic potato plants. Microbiol Res 156:75–82PubMedGoogle Scholar
  37. 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 29:365–377CrossRefGoogle Scholar
  38. 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 33:41–49CrossRefPubMedGoogle Scholar
  39. 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 32:241–247CrossRefPubMedGoogle Scholar
  40. 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 49:267–283CrossRefGoogle Scholar
  41. 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 6:393–402Google Scholar
  42. 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 68:2562–2566CrossRefPubMedGoogle Scholar
  43. 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 5:313–323Google Scholar
  44. 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 5:219–232CrossRefGoogle Scholar
  45. 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 19:803–813PubMedGoogle Scholar
  46. Oger P, Petit A, Dessaux Y (1997) Genetically engineered plants producing opines alter their biological environment. Nature Biotech 15:369–372Google Scholar
  47. 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 9:881–890CrossRefPubMedGoogle Scholar
  48. Palm CJ, Donegan KK, Harris D, Seidler RJ (1994) Quantification in soil of Bacillus thuringiensis var. kurstaki δ-endotoxin from transgenic plants. Mol Ecol 3:145–151Google Scholar
  49. Pankhurst CE, Doube BM, Gupta VVSR (1997) Biological indicators of soil health. CAB International, WallingfordGoogle Scholar
  50. 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 33:1225–1230CrossRefGoogle Scholar
  51. 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 40:29–37Google Scholar
  52. Serageldin I (1999) Biotechnology and food security in the 21st century. Science 285:387–389CrossRefPubMedGoogle Scholar
  53. 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 29:263–272CrossRefGoogle Scholar
  54. 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 44:844–851CrossRefGoogle Scholar
  55. 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 2728–2741Google Scholar
  56. 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, 1994Google Scholar
  57. 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 187–203Google Scholar
  58. Van der Putten WH, Peters BAM (1997) How soil-borne pathogens may affect plant communities. Ecology 78:1785–1795Google Scholar
  59. 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 6:261–264Google Scholar
  60. 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 61:3031–3034Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • M. Bruinsma
    • 1
  • G. A. Kowalchuk
    • 1
  • J. A. van Veen
    • 1
    Email author
  1. 1.Netherlands Institute of Ecology (NIOO-KNAW)Center for Terrestrial Ecology (CTE)HeterenThe Netherlands

Personalised recommendations