Abstract
Genetically modified microorganisms hold great promise for environmental applications. Nonetheless, some may have unintended adverse effects. Of particular concern for risk assessment is the simple fact that microorganisms are self-replicating entities, so that it may be impossible to control an adverse effect simply by discontinuing further releases of the organism. It has been suggested, however, that genetically modified microorganisms will be poor competitors and therefore unable to persist in the wild due to energetic inefficiency, disruption of genomic coadaptation, or domestication. Many studies support the hypothesis that genetically modified microorganisms are less fit than their progenitors, but there are a few noteworthy counter-examples in which genetic modifications unexpectedly enhance competitive fitness. Furthermore, subsequent evolution may eliminate the maladaptive effects of some genes, increasing the likelihood that a modified organism or its engineered genes will persist. Evaluating the likelihood that a genetically modified microorganism or its engineered genes will persist is a complex ecological and evolutionary problem. Therefore, an efficient regulatory framework would require such evaluations only when there are plausible scenarios for significant adverse environmental effects.
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References
Altmann, M., ‘Biopesticides’ turning into pests? Trends Ecol. Evol.7 (1992) 65.
Andrews, K. J., and Hegeman, G. D., Selective disadvantage of nonfunctional protein synthesis inEscherichia coli. J. molec. Evol.8 (1976) 317–328.
Bassford, P. J. Jr, Silhavy, T. J., and Beckwith, J. R., Use of gene fusion to study secretion of maltose-binding protein intoEscherichia coli periplasm. J. Bact.139 (1979) 19–31.
Bennett, A. F., and Lenski, R. E., Evolutionary adaptation to temperature. II. Thermal niches of experimental lines ofEscherichia coli. Evolution47 (1993) 1–12.
Bennett, A. F., Lenski, R. E., and Mittler, J. E., Evolutionary adaptation to temperature. I. Fitness responses ofEscherichia coli to changes in its thermal environment. Evolution46 (1992) 16–30.
Biel, S. W., and Hartl, D. L., Evolution of transposons: natural selection for Tn5 inEscherichia coli K12. Genetics103 (1983) 581–592.
Bouma, J. E., and Lenski, R. E., Evolution of a bacteria/plasmid association. Nature335 (1988) 351–352.
Brill, W. J., Safety concerns and genetic engineering in agriculture. Science227 (1985) 381–384.
Clarke, G. M., and McKenzie, J. A., Developmental stability of insecticide resistant phenotypes in blowfly; a result of canalizing natural selection. Nature325 (1987) 345–346.
Cohan, F. M., King, E. C., and Zawadzki, P., Amelioration of the deleterious pleiotropic effects of an adaptive mutation inBacillus subtilis. Evolution, in press.
Croft, B. A., and Brown, A. W. A., Responses of arthropod natural enemies to pesticides. A. Rev. Ent.20 (1975) 285–335.
DaSilva, N. A., and Bailey, J. E., Theoretical growth yield estimates for recombinant cells. Biotechnol. Bioeng.28 (1986) 741–746.
Davies, J., Genetic engineering: processes and products. Trends Ecol. Evol.3 (1988) S7-S11.
Davis, B. D., Bacterial domestication: underlying assumptions. Science235 (1987) 1329–1335.
DeBach, P., Biological Control by Natural Enemies. Cambridge University Press, London 1974.
Dykhuizen, D. E., Selection for tryptophan auxotrophs ofEscherichia coli in glucose-limited chemostats as a test of the energy conservation hypothesis of evolution. Evolution32 (1978) 125–150.
Dykhuizen, D. E., Experimental studies of natural selection in bacteria. A. Rev. ecol. Syst.21 (1990) 378–398.
Dykhuizen, D. E., Experimental evolution: replicating history. Trends Ecol. Evol.7 (1992) 250–252.
Dykhuizen, D. E., Campbell, J. H., and Rolfe, B. G., The influence of prophage on the growth rate ofE. coli. Microbios23 (1978) 99–113.
Dykhuizen, D. E., and Davies, M., An experimental model: bacterial specialists and generalists competing in chemostats. Ecology61 (1980) 876–882.
Dykhuizen, D. E., and Hartl, D. L., Selective neutrality of 6GPD allozymes inE. coli and the effects of genetic background. Genetics96 (1980) 801–817.
Dykhuizen, D. E., and Hartl, D. L., Selection in chemostats. Microbiol. Rev.47 (1983) 150–168.
Eckert, B., and Beck, C. F., Overproduction of transposon Tn10-encoded tetracycline resistance protein results in cell death and loss of membrane potential. J. Bact.171 (1989) 3557–3559.
Edlin, G., Lin, L., and Kudrna, R., Lambda lysogens ofE. coli reproduce more rapidly than non-lysogens. Nature255 (1975) 735–737.
Edlin, G., Tait, R. C., and Rodriguez, R. L., A bacteriophage Lambda cohesive ends (cos) DNA fragment enhances the fitness of plasmid-containing bacteria growing in energy-limited chemostats. Bio/Technology2 (1984) 251–254.
Futuyma, D. J., Evolutionary Biology, 2nd edn. Sinauer Associates, Sunderland, Massachusetts 1986.
Gould, F., Genetic engineering, integrated pest management and the evolution of pests. Trends Ecol. Evol.3 (1988) S15-S18.
Hartl, D. L., Dykhuizen, D. E., Miller, R. D., Green, L., and deFramond, J., Transposable element IS50 improves growth rate ofE. coli cells without transposition. Cell35 (1983) 503–510.
Ito, K., Bassford, P. J. Jr., and Beckwith, J., Protein localization inE. coli: is there a common step in the secretion of periplasmic and outer-membranes proteins? Cell24 (1991) 707–717.
Kim, J., Ginzburg, L. R., and Dykhuizen, D. E., Quantifying the risks of invasion by genetically engineered organisms, in: Assessing Ecological Risks of Biotechnology, pp. 193–214. Ed. L. R. Ginzburg. Butterworth-Heinemann, Boston 1991.
Koch, A. L., The protein burden oflac operon products. J. molec. Evol.19 (1983) 455–462.
Lenski, R. E., The infectious spread of engineered genes, in: Application of Biotechnology: Environmental and Policy Issues, pp. 99–124. Ed. J. R. Fowle, III. American Association for the Advancement of Science, Washington, D. C. 1987.
Lenski, R. E., Experimental studies of pleiotropy and epistasis inEscherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution42 (1988) 425–432.
Lenski, R. E., Experimental studies of pleiotropy and epistasis inEscherichia coli. II. Compensation for maladaptive pleiotropic effects associated with resistance to virus T4. Evolution42 (1988) 433–440.
Lenski, R. E., Quantifying fitness and gene stability in micro-organisms, in: Assessing Ecological Risks of Biotechnology, pp. 173–192. Ed. L. R. Ginzburg. Butterworth-Heinemann, Boston 1991.
Lenski, R. E., Relative fitness: its estimation and its significance for environmental applications of microorganisms, in: Microbial Ecology: Principles, Applications and Methods, pp 183–198. Eds M. Levin, R. Seidler and M. Rogul. McGraw-Hill, New York 1992.
Lenski, R. E., Experimental evolution, in: Encyclopedia of Microbialogy, Vol. 2, pp. 125–140. Ed. J. Lederberg. Acdemic Press, San Diego, California 1992.
Lenski, R. E., and Bouma, J. E., Effects of segregation and selection on instability of pACYC184 inEscherichia coli B. J. Bact.169 (1987) 5314–5316.
Lenski, R. E., and Levin, B. R., Constraints on the coevolution of bacteria and virulent phage: a model some experiments, and predictions for natural communities. Am. Nat.125 (1985) 585–602.
Lenski, R. E., and Nguyen, T. T., Stability of recombinant DNA and its effects on fitness. Trends Ecol. Evol.3 (1988) S18-S20.
Lenski, R. E., Rose, M. R., Simpson, S. C., and Tadler, S. C., Long-term experimental evolution inEscherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat.138 (1991) 1315–1341.
Levin, B. R., and Lenski, R. E., Coevolution in bacteria and their viruses and plasmids, in: Coevolution, pp. 99–127. Eds D. J. Futuyma and M. Slatkin. Sinauer Associates, Sunderland, Massachusetts 1983.
Lin, L., Bitner, R., and Edlin, G., Increased reproductive fitness ofEscherichia coli Lambda lysogens. J. Virol.21 (1977) 554–559.
McKenzie, J. A., Whitten, M. J., and Adena, M. A., The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly,Lucilia cuprina. Heredity49 (1982) 1–9.
Modi, R. I., and Adams, J., Coevolution in bacteria-plasmid populations. Evolution45 (1991) 656–667.
Moyed, H. S., Nguyen, T. T., and Bertrand, K. P., Multicopy Tn10 tet plasmids confer sensitivity to induction oftet gene expression. J. Bact.155 (1983) 549–556.
National Research Council (Committee on Scientific Evaluation of the Introduction of Genetically Modified Microorganisms and Plants into the Environment). Field Testing Genetically Modified Organisms: Framework for Decisions. National Academy Press, Washington, D. C. 1989.
Nguyen, T. N. M., Phan, Q. G., Duong, L. P., Bertrand, K. P., and Lenski, R. E. Effects of carriage and expression of the Tn10 tetracycline resistance operon on the fitness ofEscherichia coli K12. Molec. Biol. Evol.6 (1989) 213–225.
Regal, P. J., Models of genetically engineered organisms and their ecological impact, in: Ecology of Biological Invasions of North America and Hawaii, pp. 111–129. Eds H. A. Mooney and J. A. Drake. Springer-Verlag, New York 1986.
Regal, P. J., The adaptive potential of genetically engineered organisms in nature. Trends Ecol. Evol.3 (1988) S36-S38.
Tiedje, J. M., Colwell, R. K., Grossman, Y. L., Hodson, R., Lenski, R. E., Mack, R. N., and Regal, P. J., The planned introduction of genetically engineered organisms: ecological considerations and recommendations. Ecology70 (1989) 298–315.
Vogel, T. M., and McCarty, P. L., Biotransformation of tetrachloroethylene to trichloroethylene, dichloroethylene, vinyl chloride, and carbon dioxide under methanogenic conditions. Appl. envir. Microbiol.49 (1985) 1080–1083.
Woodwell, G. M., Wurster, C. F. Jr., and Isaacson, P. A., DDT residues in an east coast estuary: a case of biological concentration of a persistent pesticide. Science156 (1967) 821–823.
Zamenhof, S., and Eichhorn, H. H., Study of microbial evolution through loss of biosynthetic funtions: establishment of ‘defective’ mutants. Nature216 (1987) 456–458.
Zund, P., and Lebek, G., Generation time-prolonging R plasmids: correlation between increases in the generation time ofEscherichia coli caused by R plasmids and their molecular size. Plasmid3 (1980) 65–69.
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Lenski, R.E. Evaluating the fate of genetically modified microorganisms in the environment: Are they inherently less fit?. Experientia 49, 201–209 (1993). https://doi.org/10.1007/BF01923527
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DOI: https://doi.org/10.1007/BF01923527