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Monitoring and modeling horizontal gene transfer

Nature Biotechnology volume 22, pages 1110–1114 (2004)Cite this article

Abstract

Monitoring efforts have failed to identify horizontal gene transfer (HGT) events occurring from transgenic plants into bacterial communities in soil or intestinal environments. The lack of such observations is frequently cited in biosafety literature and by regulatory risk assessment. Our analysis of the sensitivity of current monitoring efforts shows that studies to date have examined potential HGT events occurring in less than 2 g of sample material, when combined. Moreover, a population genetic model predicts that rare bacterial transformants acquiring transgenes require years of growth to out-compete wild-type bacteria. Time of sampling is there-fore crucial to the useful implementation of monitoring. A population genetic approach is advocated for elucidating the necessary sample sizes and times of sampling for monitoring HGT into large bacterial populations. Major changes in current monitoring approaches are needed, including explicit consideration of the population size of exposed bacteria, the bacterial generation time, the strength of selection acting on the transgene-carrying bacteria, and the sample size necessary to verify or falsify the HGT hypotheses tested.

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Figure 1: Time to fixation (in bacterial generations) of a single HGT event occurring in a bacterial population of N = 1010.
Figure 2: The probability of detection of an HGT event into a bacterial population of 1010.

References

  1. Maynard Smith, J., Feil, E.J. & Smith, N.H. Population structure and evolutionary dynamics of pathogenic bacteria. Bioessays 22, 1115–1122 (2000).

    Article  Google Scholar 

  2. Ochman, H., Lawrence, J.G. & Groisman, E.A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304 (2000).

    Article  CAS  Google Scholar 

  3. Nielsen, K.M. An assessment of factors affecting the likelihood of horizontal transfer of recombinant plant DNA to bacterial recipients in the soil and phytosphere. Coll. Biosafety Rev. (Italy) 1, 96–149 (2003).

    Google Scholar 

  4. Conner, A.J, Glare, T.R. & Nap, J.-P. The release of genetically modified crops into the environment, part II. Overview of ecological risk assessment. Plant J. 33, 19–46 (2003).

    Article  Google Scholar 

  5. Nielsen, K.M, Bones, A., Smalla, K. & van Elsas, J.D. Horizontal gene transfer from transgenic plants to terrestrial bacteria—a rare event? FEMS Microbiol. Rev. 22, 79–103 (1998).

    Article  CAS  Google Scholar 

  6. Ceccherini, M.T. et al. Degradation and transformability of DNA from transgenic leaves. Appl. Environ. Microbiol. 69, 673–678 (2003).

    Article  CAS  Google Scholar 

  7. De Vries, J., Meier, P. & Wackernagel, W. The natural transformation of the soil bacteria Pseudomonas stutzeri and Acinetobacter sp. by transgenic plant DNA strictly depends on homologous sequences in the recipient cells. FEMS Microbiol. Lett. 195, 211–215 (2001).

    Article  CAS  Google Scholar 

  8. Gebhard, F. & Smalla, K. Transformation of Acinetobacter sp. strain BD413 by transgenic sugar beet DNA. Appl. Environ. Microbiol. 64, 1550–1554 (1998).

    Article  CAS  Google Scholar 

  9. Kay E. et al. In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl. Environ. Microbiol. 68, 3345–3351 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Netherwood, T. et al. Assessing the survival of transgenic plant DNA in the human gastrointestinal tract. Nat. Biotechnol. 22, 204–209 (2004).

    Article  CAS  Google Scholar 

  12. European Food Safety Authority. Opinion of the scientific panel on genetically modified organisms on the use of antibiotic resistance genes as marker genes in genetically modified plants. The EFSA J. 48, 1–18 (2004).

  13. Henscke, R.B. & Schmidt, F.R.J. Screening of soil bacteria for plasmids carrying antibiotic resistance. Biol. Fertil. Soils 9, 257–260 (1990).

    Article  Google Scholar 

  14. Shaw, K.J., Rather, P.N., Hare, R.S. & Miller, G.H. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Rev. 57, 138–163 (1993).

    Article  CAS  Google Scholar 

  15. Nielsen, K.M., van Elsas, J.D. & Smalla, K. Transformation of Acinetobacter sp. BD413(pFG4ΔnptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl. Environ. Microbiol. 66, 1237–1242 (2000).

    Article  CAS  Google Scholar 

  16. Badosa, E., Moreno, C. & Montesinos, E. Lack of detection of ampicillin resistance gene transfer from Bt176 transgenic corn to culturable bacteria under field conditions. FEMS Microbiol. Ecol. 48, 169–178 (2004).

    Article  CAS  Google Scholar 

  17. Paget, E., Lebrun, M., Freyssinet G. & Simonet, P. The fate of recombinant plant DNA in soil. Eur. J. Soil. Biol. 34, 81–88 (1998).

    Article  CAS  Google Scholar 

  18. Frostegaard, Å. et al. Quantification of bias related to the extraction of DNA directly from soils. Appl. Environ. Microbiol. 65, 5409–5420 (1999).

    Article  Google Scholar 

  19. Martin-Laurent, F. et al. DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl. Environ. Microbiol. 67, 2354–2359 (2001).

    Article  CAS  Google Scholar 

  20. Ma, J.K.-C., Drake, P.M. & Christou, P. The production of recombinant pharmaceutical proteins in plants. Nat. Rev. Genet. 4, 794–805 (2003).

    Article  CAS  Google Scholar 

  21. Elena, S.F. et al. Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102–103, 349–358 (1998).

    Article  Google Scholar 

  22. Remold, S.K. & Lenski, R.E. Pervasive joint influence of epistasis and plasticity on mutational effects in Escherichia coli. Nat. Genet. 36, 423–426 (2004).

    Article  CAS  Google Scholar 

  23. Hartl, D.L. & Clark, A.G. Principles of population genetics, edn. 3 (Sinauer Associates Inc. Sunderland, MA, USA, 1997).

    Google Scholar 

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Acknowledgements

K.M.N. received financial support from the Research Council of Norway. J.P.T. thanks the Miller Institute for Basic Research in Science for funding and administrative support. We thank M. Choi for comments on the manuscript.

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Authors and Affiliations

  1. Department of Pharmacy, Faculty of Medicine, University of Tromsø, Tromsø, N9037, Norway

    Kaare M Nielsen

  2. Norwegian Institute of Gene Ecology, Research Park, Tromsø, N9294, Norway

    Kaare M Nielsen

  3. Department of Plant & Microbial Biology, University of California, Berkeley, 947200-3102, California, USA

    Jeffrey P Townsend

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  1. Kaare M Nielsen
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Correspondence to Kaare M Nielsen.

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Nielsen, K., Townsend, J. Monitoring and modeling horizontal gene transfer. Nat Biotechnol 22, 1110–1114 (2004). https://doi.org/10.1038/nbt1006

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