A field study with genetically engineered alfalfa inoculated with recombinant Sinorhizobium meliloti: Effects on the soil ecosystem

Journal of Applied Ecology

Volumn 36, Issue 6, 1999, Pages 920-936

  Donegan, Katherine K ^a   Seidler, Ramon J ^b   Doyle, Jack D ^b,c   Porteous, L Arlene ^b   Digiovanni, George ^b,d   Widmer, Franco ^b,e   Watrud, Lidia S ^b  

^a DYNAMAC CORPORATION   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c Office of Information Services   (United States)

^d Amer Water Wk Serv Company Inc   (United States)

^e ETH ZURICH   (Switzerland)

Author keywords

Genetically engineered organisms; GMOs; Risk assessment; Soil ecology

Indexed keywords

ALFALFA; AMYLASE; ANTIBIOTIC RESISTANCE; DNA FINGERPRINTING; ENVIRONMENTAL FATE; ENVIRONMENTAL IMPACT ASSESSMENT; ENZYME ACTIVITY; GENOTYPE; INOCULATION; LIGNIN PEROXIDASE; MICROBE RESPIRATION; MICROBIAL POPULATION DYNAMICS; NITROGEN FIXATION; OXIDOREDUCTASE; PH; PLANT GROWTH; SOIL; TRANSGENIC PLANT; WILD RELATIVE;

ALFALFA; ECOLOGICAL IMPACT; INOCULATION; RHIZOBACTERIUM; SOIL ECOSYSTEM; TRANSGENIC PLANT;

ANIMALIA; ARTHROPODA; BACTERIA (MICROORGANISMS); FUNGI; MEDICAGO SATIVA; NEMATODA; PROTOZOA; RHIZOBIACEAE; RHIZOBIUM; SINORHIZOBIUM MELILOTI;

EID: 0033372288     PISSN: 00218901     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2664.1999.00448.x     Document Type: Article

References (51)

1. Alexander, M. (1982) Most probable number method for microbial populations. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties (eds A.L. Page, R.H. Miller & D.R. Keeney), pp. 815-820. American Society of Agronomy, Madison, WI.
2. Austin, A., Bingham, E.T., Mathews, D.E., Shahan, M.N., Will, J. & Burgess, R.R. (1995) Production and field performance of transgenic alfalfa (Medicago sativa L.) expressing alpha-amylase and manganese-dependent lignin peroxidase. Euphytica, 85, 381-393.
3. Baermann, G. (1917) Eine einfache Methode zur Auffindung von Akylostomum (Nematoden) Larven in erdproben. Mededlingen uit het Geneeskundig laboratorium te Weltevreden, pp. 41-47.
4. Beare, H.H., Neely, C.L., Coleman, D.C. & Hargrove, W.L. (1990) A substrate-induced respiration (SIR) method for measurement of fungal and bacterial biomass on plant residues. Soil Biology and Biochemistry, 22, 585-594.
5. Bergersen, F.J. (1961) The growth of Rhizobium in synthetic media. Australian Journal of Biological Sciences, 14, 349-360.
6. Bongers, T. (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia, 83, 14-19.
7. Borror, D.J., Triplehorn, C.A. & Johnson, N.F. (1992) An Introduction to the Study of Insects, 6th edn. Harcourt Brace College Publishers, New York, NY.
8. Bosworth, A.H., Williams, M.K., Albrecht, K.A., Kwiatkowski, R., Beynon, J., Hankinson, R.R., Ronson, C.W., Cannon, F., Wacek, R.J. & Triplett, E.W. (1994) Alfalfa yield response to inoculation with recombinant strains of Rhizobium meliloti with an extra copy of dctABD and/or modified nifA expression. Applied and Environmental Microbiology, 60, 3815-3832.
9. Chen, W.X., Van, G.H. & Yi, J.I. (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. International Journal of Systematic Bacteriology, 38, 392-397.
10. Crawford, D.L., Doyle, J.D., Wang, Z., Hendricks, C.W., Bentjen, S.A., Bolton, H. Jr, Frederickson, J.K. & Bleakley, B.H. (1993) Effects of lignin peroxidase-expressing recombinant Streptomyces liridans TR 23.1 on biogeochemical cycling and microbial numbers and activities in soil microcosms. Applied and Environmental Microbiology, 59, 508-518.
11. DiGiovanni, G.D., Watrud, L.S., Seidler, R.J. & Widmer, F. (1999a) Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using Biolog GN metabolic fingerprinting and enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Microbial Ecology, 37, 129-139.
12. DiGiovanni, G.D., Watrud, L.S., Seidler, R.J. & Widmer, F. (1999b) Fingerprinting of mixed bacterial strains and Biolog gram negative (GN) substrate communities by enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Current Microbiology, 38, 217-223.
13. Donegan, K.K., Palm, C.J., Fieland, V.J., Porteous, L.A., Ganio, L.M., Schaller, D.L., Bucao, L.Q. & Seidler, R.J. (1995) Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Applied Soil Ecology, 2, 111-124.
14. Donegan, K.K., Schaller, D.L., Stone, J.K., Ganio, L.M., Reed, G., Hamm, P.B. & Seidler, R.J. (1996) Microbial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var. tenebrionis endotoxin. Transgenic Research, 5, 25-35.
15. Donegan, K.K., Seidler, R.J., Fieland, V.J., Schaller, D.L., Palm, C.J., Ganio, L.M., Cardwell, D.M. & 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. Journal of Applied Ecology, 34, 767-777.
16. Doyle, J.D., Short, K.A., Stotzky, G., King, R.J., Seidler, R.J. & Olsen, R.H. (1991) Ecologically significant effects of Pseudomonas putida PP.0301 (pR0103), genetically engineered to degrade 2,4-dichlorophenoxyacetate, on microbial populations and processes in soil. Canadian Journal of Microbiology, 37, 682-691.
17. Doyle, J.D., Stotzky, G., McClung, G. & Hendricks, C.W. (1995) Effects of genetically engineered microorganisms on microbial populations and processes in natural habitats. Advances in Applied Microbiology, 40, 237-287.
18. Edwards, C.A. (1991) The assessment of populations of soil-inhabiting invertebrates. Agriculture, Ecosystems and Environment, 34, 145-176.
19. Embley, T.M., Finlay, B.J., Thomas, R.H. & Dyal, P.L. (1992) The use of rRNA sequences and fluorescent probes to investigate the phylogenetic positions of the anaerobic ciliate Metopus palaeformis and its archaebacterial endosymbiont. Journal of General Microbiology, 138, 1479-1487.
20. Federal Register (1986) Coordinated framework for regulation of biotechnology; announcement of policy and notice for public comment. Federal Register, 51, 23302-23393.
21. Fraley, R. (1992) Sustaining the supply. Bio/Technology, 10, 40-43.
22. Garland, J.L. (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biology and Biochemistry, 28, 213-221.
23. Garland, J.L. & Mills, A.L. (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source-utilization. Applied and Environmental Microbiology, 57, 2351-2359.
24. Giovannoni, S.J., DeLong, E.F., Olsen, G.J. & Pace, N.R. (1988) Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. Journal of Bacteriology, 170, 720-726.
25. Hendricks, C.W., Doyle, J.D. & Hugley, B. (1995) A new solid medium for enumerating cellulose-utilizing bacteria from soil. Applied and Environmental Microbiology, 61, 2016-2019.
26. Hse, S.C. & Lockwood, J.L. (1975) Powdered chitin agar as selective medium for enumeration of Actinomycete in water and soil. Applied and Environmental Microbiology, 29, 426.
27. James, N. (1958) Soil extract in soil microbiology. Canadian Journal of Microbiology, 4, 363-370.
28. King, A.D. Jr, Hocking, A.D. & Pitt, J.I. (1979) Dichoranrose bengal medium for enumeration and isolation of molds from foods. Applied and Environmental Microbiology, 37, 959-964.
29. Lane, D.J. (1991) 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics (eds E. Stackebrandt & M. Goodfellow), pp. 115-147. John Wiley & Sons Ltd, Chichester, UK.
30. Levin, M.A. & Israeli, E. (1996) Engineered Organisms in Environmental Settings - Biotechnological and Agricultural Applications. CRC Press, Boca Raton, FL.
31. Massol-Deya, A., Weller, R., Rios-Hernandez, L., Zhou, J.Z., Hickey, R.F. & Tiedje, J.M. (1997) Succession and convergence of biofilm communities in fixed-film reactors treating aromatic hydrocarbons in ground-water. Applied and Environmental Microbiology, 63, 270-276.
32. Oger, P., Petit, A. & Dessaux, Y. (1997) Genetically engineered plants producing opines alter their biological environment. Nature Biotechnology, 15, 369-372.
33. Oregon State University (1989) Methods of Soil Analysis Used in the Soil Testing Laboratory at Oregon State University. Agriculture Experiment Station, Oregon State University, Corvallis, OR.
34. Paul, E.A. & Clark, F.E. (1989) Soil Microbiology and Biochemistry. Academic Press Inc., New York, NY.
35. Porteous, L.A., Seidler, R.J. & Watrud, L.S. (1997) An improved method for purifying DNA from soil for polymerase chain reaction amplification and molecular ecology applications. Molecular Ecology, 6, 787-791.
36. SAS Institute Inc. (1989) SAS/STAT Users' Guide, Version 6, Vol. 1, 4th edn. SAS Institute Inc., Cary, NC.
37. Savka, M.A. & Farrand, S.K. (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nature Biotechnology, 15, 363-368.
38. Seidler, R. & Levin, M. (1994) Potential ecological and nontarget effects of transgenic plant gene products on agriculture, silviculture, and natural ecosystems: general introduction. Molecular Ecology, 3, 1-3.
39. Seidler, R.J., Watrud, L.S. & George, S.E. (1998) Assessing risks from GMO's to ecosystems and human health. Handbook of Environmental Risk Assessment and Management (ed. P. Calow), pp. 110-146. Blackwell Science, Oxford, UK.
40. Short, K.A., Doyle, J.D., King, R.J., Seidler, R.J., Stotzky, G. & Olsen, R.H. (1991) Effects of 2,4-dichlorophenol, a metabolite of a genetically engineered bacterium, and 2, 4-dichlorophenoxyacetate on some microorganism-mediated ecological processes in soil. Applied and Environmental Microbiology, 57, 412-418.
41. Skujiins, J. (1976) Extracellular enzymes in soil. CRC Critical Reviews in Microbiology, 4, 383-421.
42. Speir, T.W. & Ross, D.J. (1978) Soil phosphatase and sulphatase. Soil Enzymen (ed. R.G. Burns), pp. 197-250. Academic Press, New York, NY.
43. Stotzky, G., Broder, M.W., Doyle, J.D. & Jones, R.A. (1993) Selected methods for the detection and assessment of ecological effects resulting from the release of genetically engineered microorganisms to the terrestrial environment. Advances in Applied Microbiology, Vol. 38 (eds S. Neidleman & A.I. Laskin), pp. 1-99. Academic Press, New York, NY.
44. Tabatabai, M.A. (1994) Soil enzymes. Part 2. Microbiological and Biochemical Properties (ed. S.H. Mickelson), pp. 775-833. Soil Science Society of America, Madison, WI.
45. Tullgren, A. (1918) Ein sehr einfacher Ausleseapparat terricle Tierformen. Zeitschrift Für Angewandte Entomologie, 4, 149-150.
46. US EPA (1992) Monitoring Small-Scale Field Tests of Microorganisms. Prevention, Pesticides, and Toxic Substances (TS-788). EPA/700/R-92/008. US Environmental Protection Agency, Washington, DC.
47. Watrud, L.S. & Seidler, R.J. (1998) Non-target ecological effects of plant, microbial, and chemical introductions to terrestrial systems. Soil Chemistry and Ecosystem Health (ed. P.M. Huang), pp. 313-340. Soil Science Society of American, Madison, WI.
48. 2-fixing abilities during a multiyear field trial with transgenic alfalfa. Proceedings of the Fifth International Symposium on the Biosafety Results of Field Tests of Genetically Modified Plants and Microorganisms Biologische Bundesanstalt für Land und Forstwirtschaft, Stadthalle, Braunschweig, Germany, (in press).
49. Widmer, F., Seidler, R.J., Watrud, L.S. & DiGiovanni, G.D. (1998) A highly selective PCR protocol for detecting 16S rRNA genes of the genus Pseudomonas (sensu stricto) in environmental samples. Applied and Environmental Microbiology, 64, 2545-2553.
50. Yeates, G.W., Bongers, R., De Goede, R.G.M., Freckman, D.W. & Georgeiva, S.S. (1993) Feeding habits in soil nematodes families and genera - an outline for soil ecologists. Journal of Nematology, 25, 315-331.
51. Young, C.C., Burghoff, R.L., Keim, L.G., Minak-Bernero, V., Lute, J.R. & Hinton, S.M. (1993) Polyvinylpyrrolidone-agarose gel electrophoresis purification of polymerase chain reaction-amplifiable DNA from soils. Applied and Environmental Microbiology, 59, 1972-1974.