Skip to main content

Advertisement

Log in

Microbial diversity in soil: ecological theories, the contribution of molecular techniques and the impact of transgenic plants and transgenic microorganisms

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

Abstract

This review mainly discusses three related topics: the application of ecological theories to soil, the measurement of microbial diversity by molecular techniques and the impact of transgenic plants and microorganisms on genetic diversity of soil. These topics were debated at the Meeting on Soil Emergency held in Erice (Trapani, Italy) in 2001 for the celebration of the 50th anniversary of the Italian Society of Soil Science. Ecological theories have been developed by studying aboveground ecosystems but have neglected the belowground systems, despite the importance of the latter to the global nutrient cycling and to the presence of life on the Earth. Microbial diversity within the soil is crucial to many functions but it has been difficult in the past to determine the major components. Traditional methods of analysis are useful but with the use of molecular methods it is now possible to detect both culturable and unculturable microbial species. Despite these advances, the link between microbial diversity and soil functions is still a major challenge. Generally studies on genetically modified bacteria have not addressed directly the issue of microbial diversity, being mainly focused on their persistence in the environment, colonization ability in the rhizosphere, and survival. Concerns have been raised that transgenic plants might affect microbial communities in addition to environmental factors related to agricultural practice, season, field site and year. Transgenic plant DNA originating from senescent or degraded plant material or pollen has been shown to persist in soil. Horizontal transfer of transgenic plant DNA to bacteria has been shown by the restoration of deleted antibiotic resistance genes under laboratory in filter transformations, in sterile soil or in planta. However, the transformation frequencies under field conditions are supposed to be very low. It is important to underline that the public debate about antibiotic resistant genes in transgenic plants should not divert the attention from the real causes of bacterial resistance to antibiotics, such as the continued abuse and overuse of antibiotics prescribed by physicians and in animal husbandry.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

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

    Google Scholar 

  • Alfreider A, Peters S, Tebbe CC, Rangger A, Insam H (2002) Microbial community dynamics during composting of organic matter as determined by 16S ribosomal DNA analysis. Compost Sci Util 10:303–312

    Google Scholar 

  • Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Atlas RM, Bartha R (1998) Microbial ecology. Fundamentals and applications, 4th edn. Addison-Wesley, Reading

    Google Scholar 

  • Avaniss-Aghajani E, Jones K, Chapman D, Brunk C (1994) A molecular technique for identification of bacteria using small subunit ribosomal RNA sequences. Biotechniques 17:144–146

    CAS  PubMed  Google Scholar 

  • Basaglia M, Casella S, Peruch U, Poggiolini S, Vamerali T, Mosca G, Vanderleyden J, De Troch P, Nuti MP (2003) Field release of genetically marked Azospirillum brasiliense in association with Sorghum dicolor L. Plant Soil 256:281–290

    Article  CAS  Google Scholar 

  • Bending GT, Turner MK, Jones JE (2002) Interactions between crop residues and soil organic matter quality and the functional diversity of soil microbial. Soil Biol Biochem 34:1037–1082

    Article  Google Scholar 

  • Bertolla F, Simonet P (1999) Horizontal gene transfer in the environment: natural transformation as a putative process for gene transfer between transgenic plants and microorganisms. Res Microbiol 150:375–384

    Google Scholar 

  • Bertolla F, van Gijsegem F, Nesmer X, Simonet P (1997) Conditions for natural transformation of Ralstonia solanacearum. Appl Environ Microbiol 63:4965–4968

    Google Scholar 

  • Bertolla F, Frostegard A, Brito B, Nesmer X, Simonet P (1999) During infection of its host, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material. Mol Plant Microbe Interact 12:467–472

    CAS  Google Scholar 

  • Blum SAG, Lorenz MG, Wackernagel W (1997) Mechanisms of retarded DNA degradation and prokaryotic origin of DNases in nonsterile soils. Syst Appl Microbiol 20:513–521

    Google Scholar 

  • Borneman J, Triplett EW (1997) Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63:2647–2653

    PubMed  Google Scholar 

  • Borneman J, Skroch PW, O’Sullivan KM, Palus JA, Rumjanek NG, Jansen JL, Nienhuis J, Triplett EW (1996) Molecular microbial diversity of an agricultural soil in Wisconsin. Appl Environ Microbiol 62:1935–1943

    CAS  PubMed  Google Scholar 

  • Brønstad K, Drønen K, Øvreås L, Torsvik V (1996) Phenotypic diversity and antibiotic resistance in soil bacterial communities. J Ind Microbiol Biotechnol 17:253–259

    Google Scholar 

  • Bruce KD (1997) Analysis of mer gene subclasses within bacterial communities in soils and sediments resolved by fluorescent-PCR-restriction fragment length polymorphism profiling. Appl Environ Microbiol 63:4914–4919

    Google Scholar 

  • de Bruijn FJ (1992) Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol 58:2180–2187

    Google Scholar 

  • Burkhardt C, Insam H, Hutchinson TC, Reber HH (1993) Impact of heavy metals on the degradative capabilities of soil bacterial communities. Biol Fertil Soils 16:154–156

    CAS  Google Scholar 

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

    Google Scholar 

  • Chatzinotas A, Sandaa R-A, Hahn D, Schönhuber W, Daae FL, Torsvik V, Zeyer J, Amann R (1998) Studies on bacterial diversity in bulk soils using different molecular techniques. Syst Appl Microbiol 21:588–592

    Google Scholar 

  • Cheneby D, Philippot L, Hartmann A, Henault C, Germon JC (2000) 16S rDNA analysis for characterization of denitrifying bacteria isolated from three agricultural soils. FEMS Microbiol Ecol 34:121–128

    Article  CAS  PubMed  Google Scholar 

  • Corich V, Giacomini A, Concheri G, Tritzerfeld B, Vendramin E, Struffi P, Basaglia M, Squartini A, Casella S, Nuti M.P, Peruch U, Poggiolini S, De Troch P, Vanderleyden J, Fedi S, Fention A, Moenne-Loccoz Y, Dowling DN, O’Gara F (1995) Environmental impact of genetically modified Azospirillum brasilense, Pseudomonas fluorescens and Rhizobium leguminosarum released as soil/seed inoculants. In: Jones D (ed) Biosafety results of field tests with genetically modified plants and microorganisms. USDA-UCLA Publ., Monterey, CA. USA pp 371–378

  • Corich V, Bosco F, Giacomini A, Basaglia M, Squartini A, Nuti MP (1996) Fate of genetically modified Rhizobium leguminosarum biovar viciae during prolonged storage of commercial inoculants. J Appl Bacteriol 81:319–328

    CAS  PubMed  Google Scholar 

  • Da Silva KRA, Salles JF, Seldin L, van Elsas JD (2003) Application of a novel Paenibacillus-specific PCR-DGGE method and sequence analysis to assess the diversity of Paenibacillus spp. in the maize rhizosphere. J Microbiol Methods 54:213–231

    Article  PubMed  Google Scholar 

  • Degens BP, Harris JA (1997) Developments of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320

    Article  CAS  Google Scholar 

  • De Leij FAAM, Bailey MJ, Whipps JM, Thompson IP, Bramwell PA, Lynch JM (1998a) Gene release and biomonitoring. In: Lynch J, Wiseman A (eds) Environmental biomonitoring. The biotechnology, ecotoxicology interface. Cambridge University Press, Cambridge, pp 70–100

    Google Scholar 

  • De Leij FAAM, Thomas CE, Bailey MJ, Whipps JM, Lynch JM (1998b) Effect of insertion site and metobolic load on the environmental fitness of a genetically modified Pseudomonas fluorescens. Appl Environ Microbiol 64:2634–2638

    PubMed  Google Scholar 

  • Demanèche S, Bertolla F, Buret F, Nalin R, Sailand A, Auriol P, Vogel TM, Simonet P (2001a) Laboratory-scale evidence for lightning-mediated gene transfer in soil. Appl Environ Microbiol 67:3440–3444

    Google Scholar 

  • Demanèche S, Kay E, Gourbière F, Simonet P (2001b) Natural transformation of Pseudomonas fluorescens and Agrobacterium tumefaciens in soil. Appl Environ Microbiol 67:2617–2621

    Google Scholar 

  • De Vries J, Wackernagel W (1998) Detection of nptII (kanamycin resistance) genes in genomes of transgenic plants by marker-rescue transformation. Mol Gen Genet 257:606–613

    Article  PubMed  Google Scholar 

  • De Vries J, Wackernagel W (2002) Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination. Proc Natl Acad Sci 99:2094–2099

    Article  PubMed  Google Scholar 

  • De Vries J, Harms K, Broer I, Kriete G, Mahn A, Düring K, Wackernagel W (1999) The bacteriolytic activity in transgenic potatoes expressing a chimeric T4 lysozyme gene and the effect of T4 lysozyme on soil- and phytopathogenic bacteria. Syst Appl Microbiol 22:280–286

    Google Scholar 

  • De Vries J, Meier P, Wackernagel W (2001) 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

    Article  PubMed  Google Scholar 

  • De Vries J, Heine M, Harms K, Wackernagel W (2003) Spread of recombinant DNA by roots and pollen of transgenic potato plants, identified by highly specific biomonitoring using natural transformation of an Acinetobacter sp. Appl Environ Microbiol 69:4455–4462

    Google Scholar 

  • Dighton J, Jones HE, Robinson CH, Beckett J (1997) The role of abiotic factors, cultivation practices and soil fauna in the dispersal of genetically modified microorganisms in soils. Appl Soil Ecol 5:109–131

    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, Seidler RJ, Doyle JD, Porteus LA, Di Giovanni 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 

  • Dröge M, Pühler A, Selbitschka W (2000) Phenotypic and molecular characterization of conjugative antibiotic resistance plasmids isolated from bacterial communities of activated sludge. Mol Gen Genet 263:471–482

    Article  PubMed  Google Scholar 

  • Drønen AK, Torsvik V, Goksøyr J, Top EM (1998) Effect of mercury addition on plasmid incidence and gene mobilizing capacity in bulk soil. FEMS Microbiol Ecol 27:381–394

    Google Scholar 

  • Duineveld BM, Kowalchuk GA, Keijzer A, van Elsas JD, van Veen JA (2001) Analysis of bacterial communities in the rhizosphere of Chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl Environ Microbiol 67:172–178

    Google Scholar 

  • Dunbar J, Ticknor LO, Kuske CR (2000) Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl Environ Microbiol 66:2943–2950

    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 38:1–9

    Article  CAS  Google Scholar 

  • Düring K, Mahn A (1999) Freisetzung und Resistenzprüfung transgener Lysozym-Kartoffeln. In: Schiemann J (ed) Freisetzungsbegleitende Sicherheitsforschung mit gentechnisch veränderten Pflanzen und Mikroorganismen. Proceedings of the BMBF Workshop on Biological Safety, 25–26 May 1998. BEO, Braunschweig, pp 39–44

    Google Scholar 

  • Escara JF, Hutton JR (1980) Thermal stability and renaturation of DNA in dimethyl sulfoxide solutions: acceleration of the renaturation rate. Biopolymers 19:1315–1327

    CAS  PubMed  Google Scholar 

  • Fægri A, Torsvik VL, Goksøyr J (1977) Bacterial and fungal activities in soil: separation of bacteria and fungi by a rapid fractionated centrifugation technique. Soil Biol Biochem 9:105–112

    Article  Google Scholar 

  • Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636

    Google Scholar 

  • Gallori E, Bazzicalupo M, Dal Canto L, Fani R, Nannipieri P, Vettori C, Stotzky G (1994) Transformation of Bacillus subtilis by DNA bound on clay in non-sterile soil. FEMS Microbiol Ecol 15:119–126

    Article  CAS  Google Scholar 

  • Garbeva P, van Veen JA, van Elsas JD (2003) Predominant Bacillus spp. in agricultural soil under different management regimes via PCR-DGGE. Microb Ecol 45:302–316

    Article  CAS  PubMed  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    Google Scholar 

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

    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 

  • Gelsomino A, Keijzer-Wolters A, Cacco G, van Elsas JD (1999) Assessment of bacterial community structure in soil by polymerase chain reaction and denaturing gradient gel electrophoresis. J Microbiol Methods 38:1–15

    Article  CAS  PubMed  Google Scholar 

  • Giller KE, Beare MH, Lavelle P, Izac A-M, Swift MJ (1997) Agricultural intensification, soil biodiversity and agroecosystem function. Appl Soil Ecol 6:3–16

    Article  Google Scholar 

  • Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles MR, Rondon MR, Clardy J, Goodman RM, Handelsman J (2002) Isolation of antibiotics Turbomycin A and B from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 68:4301–4306

    Google Scholar 

  • Gomes NCM, Heuer H, Schönfeld J, Costa R, Hagler-Mendonca L, Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180

    Article  CAS  Google Scholar 

  • Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendonça-Hagler L, Smalla K (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 69:3758–3766

    Google Scholar 

  • Griffiths BS, Ritz K, Weatley RE (1997) Relationship between functional diversity and genetic diversity in complex microbial communities. In: Insam H, Rangger A (eds) Microbial communities, functional versus structural approaches. Springer, Berlin Heidelberg New York, pp 1–18

    Google Scholar 

  • Griffiths BS, Ritz K, Bardgett RD, Cook R, Christensen S, Ekelund F, Sorensen SJ, Baath E, Bloem J, de Ruiter PC, Dolfing J, Nicolardot B (2000) Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship. Oikos 90:279–294

    Article  CAS  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 

  • Hadrys H, Balick M, Schierwater B (1992) Applications of random amplified polymorphic DNA (RAPD) in molecular ecology. Mol Ecol 1:55–63

    PubMed  Google Scholar 

  • Hahn D, Amann RI, Ludwig W, Akkermans ADL, Schleifer KH (1992) Detection of microorganisms in soil after in situ hybridization with rRNA-targeted, fluorescently labelled oligonucleotides. J Gen Microbiol 138:879–887

    Google Scholar 

  • Hall SJ, Gray SA, Hammett ZL (2000) Biodiversity-productivity relations: an experimental evaluation of mechanisms. Oecologia 122:545–555

    Article  Google Scholar 

  • Harris D (1994) Analyses of DNA extracted from microbial communities. In: Ritz K, Dighton J, Giller KE (eds) Beyond the biomass. British Society of Soil Science, Sayce, Wiley, Chichester, pp 111–118

    Google Scholar 

  • Heuer H, Smalla K (1997a) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) for studying soil microbial communities. In: van Elsas JD, Wellington EMH, Trevors JT (eds) Modern soil microbiology. Dekker, New York, pp 353–373

    Google Scholar 

  • Heuer H, Smalla K (1997b) Evaluation of community level catabolic profiling using BIOLOG GN microplates to study microbial community changes in potato phyllosphere. J Microbiol Methods 30:49–61

    Google Scholar 

  • Heuer H, Hartung K, Wieland G, Kramer I, Smalla K (1999) Polynucleotide probes that target a hypervariable region of 16S rRNA genes to identify bacterial isolates corresponding to bands of community fingerprints. Appl Environ Microbiol 65:1045–1049

    Google Scholar 

  • Heuer H, Kroppenstedt RM, Lottmann J, Berg G, Smalla K (2002a) 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

    Google Scholar 

  • Heuer H, Krögerrecklenfort E, Egan S, van Overbeek LS, Guillaume G, Nikolakopoulou TL, Wellington EMH, van Elsas JD, Collard J-M, Karagouni AD, Smalla K (2002b) Gentamycin resistance genes in environmental bacteria: prevalence and transfer. FEMS Microbiol Ecol 42:289–302

    Article  CAS  Google Scholar 

  • Holben WE, Harris D (1995) DNA-based monitoring of total bacterial community structure in environmental samples. Mol Ecol 4:627–631

    CAS  PubMed  Google Scholar 

  • Horz HP, Yimga MT, Liesack W (2001) Detection of methanotroph diversity on roots of submerged rice plants by molecular retrieval of pmoA, mmoX, mxaF, and 16S rRNA and ribosomal DNA, including pmoA-based terminal restriction fragment length polymorphism profiling. Appl Environ Microbiol 67:4177–4185

    Google Scholar 

  • Insam H (2001) Development in soil microbiology since mid 1960s. Geoderma 100:389–402

    Article  CAS  Google Scholar 

  • James C (2003) Global review of commercialized transgenic crops: 2002. ISAA Briefs 29:3–38

    Google Scholar 

  • Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J-M (2002) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils

  • Johnsen K, Jacobsen CS, Torsvik V, Sørensen J (2001) Pesticide effects on bacterial diversity in agricultural soils—a review. Biol Fertil Soils 33:443–453

    Article  Google Scholar 

  • Keel C, Schnider U, Maurhofer M, Voisard C, Burger U, Haas D, Defago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol Plant Microbe Interact 5:4–13

    CAS  Google Scholar 

  • Kowalchuk GA, Gerards S, Woldendorp JW (1997) Detection and characterization of fungal infections of Ammophila arenaria (Marran grass) roots by denaturing gradient gel electrophoresis of specifically amplified 18S rDNA. Appl Environ Microbiol 63:3858–3865

    Google Scholar 

  • Kowalchuk GA, Bruinsma M, van Veen JA (2003) Assessing responses of soil microorganisms to GM plants. Trends Ecol Evol 18:403–410

    Article  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci 82:6955–6959

    CAS  PubMed  Google Scholar 

  • Latour X, Philippot L, Corberand T, Lemanceau P (1996) The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type. FEMS Microbiol Ecol 30:163–170

    Article  Google Scholar 

  • Lee DH, Zo YG, Kim SJ (1996) Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single strand conformation polymorphism. Appl Environ Microbiol 62:3112–3120

    CAS  PubMed  Google Scholar 

  • Levy SB (1997) Antibiotic resistance: an ecological imbalance. In: Antibiotic resistance: origins, evolution, selection and spread, Ciba Foundation Symposium 207. Wiley, Chichester, pp 1–14

    Google Scholar 

  • Liesack W, Stackebrandt E (1992) Occurrence of novel groups of the domain bacteria as revealed by analysis of genetic material isolated from an Australian terrestrial environment. J Bacteriol 174:5072–5078

    CAS  PubMed  Google Scholar 

  • Liu W-T, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522

    CAS  PubMed  Google Scholar 

  • Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston DU, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  CAS  PubMed  Google Scholar 

  • Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602

    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 Microbial Ecol 33:41–49

    Article  Google Scholar 

  • Loy A, Horn M, Wagner M (2003) probeBase—an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res 31:514–516

    Article  CAS  PubMed  Google Scholar 

  • Lynch JM (2002a) Effect of living modified organisms on the soil. In: Roseland CR (ed) LMOs and the environment. United States Department of Agriculture, Md.

  • Lynch JM (2002b) Resilience of the rhizosphere to anthropogenic disturbance. Biodegradation 13:21–27

    Article  CAS  PubMed  Google Scholar 

  • MacArthur RH (1955) Fluctuations of animal populations, and a measure of stability. Ecology 36:533–536

    Google Scholar 

  • Madigan MT, Martinko JM, Parker J (2003) Brock biology of microorganisms, 10th edn. Pearson Education, Prentice Hall, Upper Saddle River, Toronto

    Google Scholar 

  • Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600

    Article  CAS  Google Scholar 

  • Marsh TL, Saxman P, Cole J, Tiedje J (2000) Terminal restriction fragment length polymorphism analysis program, a web-based research tool for microbial community analysis. Appl Environ Microbiol 66:3616–3620

    Google Scholar 

  • Massol-Deya AA, Odelson DA, Hickey RF, Tiedje JM (1995) Bacterial community fingerprinting of amplified 16S and 16-23S ribosomal DNA gene sequences and restriction endonuclease analysis (ARDRA). In: Akkermans ADL, van Elsas JD, deBruijn FJ (eds) Molecular microbial ecology manual. Kluwer, Dordrecht, pp 1–8

    Google Scholar 

  • May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • May RM (ed) (1976) Theoretical ecology, principles and applications. Blackwell, Oxford

  • McGrath SP, Chaudri AM, Giller KE (1995) Long-term effects of land application of sewage sludge: Soils, microorganisms, and plants. J Ind Microbiol 14:94–104

    CAS  PubMed  Google Scholar 

  • McNaughton SJ (1988) Diversity and stability. Nature 333:204–205

    Article  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek J Microbiol Serol 73:127–141

    Article  CAS  Google Scholar 

  • Muyzer G, de Waal ED, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  Google Scholar 

  • Nagpal ML, Fox KF, Fox A (1998) Utility of 16S–23S rRNA spacer region methodology: how similar are interspace regions within a genome and between strains for closely related organisms? J Microbiol Methods 33:211–219

    Article  CAS  Google Scholar 

  • Nakatsu CH, Torsvik V, Øvreås L (2000) Soil community analysis using DGGE of 16S rDNA polymerase chain reaction products. Soil Sci Soc Am J 64:1382–1388

    CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Loretta L, Giacomo P, Giancarlo R (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Naseby DC, Lynch JM (2002) Enzymes and micro-organisms in the rhizosphere. In: Dick RP, Burns R (eds) Enzymes in the environment. Dekker, New York, pp 109–123

    Google Scholar 

  • Nielsen KM, van Weerelt DM, Berg TN, Bones AM, Hagler AN, van Elsas JD (1997a) Natural transformation and availability of transforming chromosomal DNA to Acinetobacter calcoaceticus in soil microcosms. Appl Environ Microbiol 63:1945–1952

    Google Scholar 

  • Nielsen KM, Bones AM, van Elsas JD (1997b) Induced natural transformation of Acinetobacter calcoaceticus in soil microcosms. Appl Environ Microbiol 63:3972–3977

    Google Scholar 

  • Nielsen KM, Gebhard F, Smalla K, Bones AM, van Elsas JD (1997c) Evaluation of possible horizontal gene transfer from transgenic plants to the soil bacterium Acinetobacter calcoaceticus BD413. Theor Appl Genet 95:815–821

    Article  CAS  Google Scholar 

  • Nielsen KM, Bones AM, Smalla K, van Elsas JD (1998) Horizontal gene transfer from transgenic plants to terrestrial bacteria-a rare event? FEMS Microbiol Rev 22:79–103

    Article  CAS  PubMed  Google Scholar 

  • Nielsen KM, Smalla K, van Elsas JD (2000a) Natural transformation of Acinetobacter sp. strain BD413 with cell lysates of Acinetobacter sp., Pseudomonas fluorescens, and Burkholderia cepacia in soil microcosms. Appl Environ Microbiol 66:206–212

    Google Scholar 

  • Nielsen KM, van Elsas JD, Smalla K (2000b) Transformation of Acinetobacter sp. strain BD413 (pFG4ΔnptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl Environ Microbiol 66:1237–1242

    Google Scholar 

  • Nielsen KM, Choi M, Pietramellara G, Nannipieri P, Bensasson D (in press) Extracellular DNA: persistence in various environments and availability to bacteria. In: Schink B, Vincent W, Van Elsas JD (eds) Advances in microbial ecology. Kluwer, New York

    Google Scholar 

  • Normander B, Prosser J (2000) Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl Environ Microbiol 66:4372–4377

    Google Scholar 

  • Nüsslein K, Tiedje JM (1998) Characterization of the dominant and rare members of a young Hawaian soil bacterial community with small-subunit ribosomal DNA amplified from DNA fractionated on the basis of its guanine and cytosine composition. Appl Environ Microbiol 64:1283–1289

    Google Scholar 

  • Nuti MP (1994) Biosafety of genetically modified soil microbial inoculants. BRIDGE Programme, CEC ELWW/DGXII, Brussels, pp 1–11

  • Nuti MP, Sirsi E (2003) Science/legislation interface. In: Migheli Q, Ruiz Sanz JE (eds) Quality control and efficacy assessment of microbial inoculants, COST 830/E, Europlomas. European Commission, Brussels

    Google Scholar 

  • Odum EP (1969) The strategy of ecosystem development. Science 164:262–270

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ohtonen R, Aikio S, Vare H (1997) Ecological theories in soil biology. Soil Biol Biochem 29:1613–1619

    Article  CAS  Google Scholar 

  • Osborn AM, Moore ER, Timmis KN (2000) An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2:39–50

    Google Scholar 

  • Øvreås L, Torsvik V (1998) Microbial diversity and community structure in two different agricultural soil communities. Microb Ecol 36:306–315

    Google Scholar 

  • Øvreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Sælenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373

    Google Scholar 

  • Øvreås L, Jensen S, Daae FL, Torsvik V (1998) Microbial community changes in a perturbed agricultural soil investigated by molecular and physiological approaches. Appl Environ Microbiol 64:2739–2742

    Google Scholar 

  • Paget E, Simonet P (1994) On the track of natural transformation in soil. FEMS Microbiol Ecol 15:109–118

    Article  CAS  Google Scholar 

  • Paget E, Simonet P (1997) Development of engineered genomic DNA to monitor the natural transformation of Pseudomonas stutzeri in soil-like microcosms. Can J Microbiol 43:78–84

    Google Scholar 

  • Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–3101

    Google Scholar 

  • Perreten V, Schwarz F, Cresta L, Boeglin M, Dasen G, Teuber M (1997) Antibiotic resistance spread in food. Nature 389:801–802

    Article  CAS  Google Scholar 

  • Pukall R, Brambilla E, Stackebrandt E (1998) Automated fragment length analysis of fluorescently labeled 16S rDNA after digestion with 4-base cutting restriction enzymes. J Microbiol Methods 32:55–63

    Article  CAS  Google Scholar 

  • Ranjard L, Brothier E, Nazaret S (2000a) Sequencing bands of RISA fingerprints for the characterization and the microscale distribution of soil bacterial populations responding to mercury spiking. Appl Environ Microbiol 66:5334–5339

    Google Scholar 

  • Ranjard L, Poly F, Nazaret S (2000b) Monitoring complex bacterial communities using culture-independent molecular techniques: application to soil environment. Res Microbiol 151:167–177

    Article  CAS  PubMed  Google Scholar 

  • Ranjard L, Poly F, Lata J-C, Moguel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    Google Scholar 

  • Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of Methanogens. Appl Environ Microbiol 60:1232–1240

    Google Scholar 

  • Resca R, Basaglia M, Poggiolini S, Vian P, Bardin S, Walsh UF, Enriquez Barreiros CM, O’Gara F, Nuti MP, Casella S, Peruch U (2001) An integrated approach for the evaluation of biological control of the complex Polymyxa betae/beet necrotic yellow vein virus, by means of seed inoculants. Plant Soil 232:215–226

    Article  CAS  Google Scholar 

  • Ritz K, Griffiths BS, Torsvik VL, Hendriksen NB (1997) Analysis of soil and bacterioplancton community DNA by melting profiles and reassociation kinetics. FEMS Microbiol Lett 149:151–156

    Article  CAS  Google Scholar 

  • Rondon MR, Raffel SJ, Goodman RM, Handelsman J (1999) Toward functional genomics in bacteria: analysis of gene expression in Escherichia coli from a bacterial artificial chromosome library of Bacillus cereus. Proc Natl Acad Sci USA 96:6451–6455

    Article  CAS  PubMed  Google Scholar 

  • Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, MacNeil IA, Minor C, Tiong CL, Gilman M, Osburne MS, Clardy J, Handelsman J, Goodman RM (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 66:2541–2547

    Article  CAS  PubMed  Google Scholar 

  • Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N (1985) Enzymatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350–1354

    Google Scholar 

  • Salles JF, De Souza FA, van Elsas JD (2002). Molecular method to assess the diversity of Burkholderia species in environmental samples. Appl Environ Microbiol 68:1595–1603

    Google Scholar 

  • Salyers A (1996) The real threat from antibiotics. Nature 384:304

    Article  CAS  PubMed  Google Scholar 

  • Sandaa R-A, Enger Ø, Torsvik V (1999a) Abundance and diversity of Archaea in heavy-metal contaminated soils. Appl Environ Microbiol 65:3293–3297

    Google Scholar 

  • Sandaa R-A, Torsvik V, Enger Ø, Daae FL, Castberg T, Hahn D (1999b) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251

    Article  CAS  PubMed  Google Scholar 

  • Sandaa R-A, Torsvik V, Enger Ø (2001) Influence of long-term heavy-metal contamination on microbial communities in soil. Soil Biol Biochem 33:287–295

    Article  CAS  Google Scholar 

  • Saxena D, Stotzky G (2000) Insecticidal toxin from Bacillus thuringensis is released from roots of transgenic Bt corn in vitro and in situ. FEMS Microbial Ecol 33:35–39

    Article  CAS  Google Scholar 

  • Schlüter K, Fütter J, Potrykus I (1995) Horizontal gene transfer from a transgenic potato line to a bacterial pathogen (Erwinia chrysanthemi) occurs—if at all—at an extremely low frequency. Nat Biotechnol 13:94–98

    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

    Article  CAS  Google Scholar 

  • Schwieger F, Tebbe CC (1998) A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870–4876

    CAS  PubMed  Google Scholar 

  • Schwieger F, Tebbe CC (2000) Effect of field inoculation with Sinorhizobium meliloti L33 on the composition of bacterial communities in rhizospheres of a target plant (Medicago sativa) and a non-target plant (Chenopodium album)-linking of 16S rRNA gene-based single-strand conformation polymorphism community profiles to the diversity of cultivated bacteria. Appl Environ Microbiol 66:3556–3565

    Google Scholar 

  • Sessitsch A, Kan F-Y, Pfeifer U (2003) Diversity and community structure of culturable Bacillus spp. populations in the rhizosphere of transgenic potatoes expressing the lytic peptide cecropin B. Appl Soil Ecol 22:149–158

    Article  Google Scholar 

  • Shanahan P, O’Sullivan DJ, Simpson P, Gennor JD, O’Gara F (1992) Isolation of 2,4-diocetylphloragtuinal from a fluourescent pseudomonal and investigation of physiological parameters influencing production. Appl Environ Microbiol 58:353–358

    CAS  Google Scholar 

  • Shannon CE, Weaver W (1969) The mathematical theory of communication. University of Illinois Press, Urbana, Ill.

    Google Scholar 

  • Sharma S, Piccolo A, Insam H. (1997) Different carbon source utilization profiles from four tropical soils of Ethiopia. In: Insam H, Rangger A (eds) Microbial communities. Functional versus structural approaches. Springer, Berlin Heidelberg New York, pp 132-139

  • 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 

  • Sikorski J, Graupner S, Lorenz MG, Wackernagel W (1998) Natural transformation of Pseudomonas stutzeri in a non-sterile soil. Microbiology 144:569–576

    Google Scholar 

  • Smalla K, van Overbeek LS, Pukall R, van Elsas JD (1993) Prevalence of nptII and Tn5 in kanamycin resistant bacteria from different environments. FEMS Microbiol Ecol 13:47–58

    Article  CAS  Google Scholar 

  • Smalla K, Wachtendorf U, Heuer H, Liu W-T, Forney L (1998) Analysis of BIOLOG GN substrate utilization patterns by microbial communities. Appl Environ Microbiol 64:1220–1225

    CAS  Google Scholar 

  • Smalla K, Heuer H, Götz A, Niemeyer D, Krögerrecklenfort E, Tietze E (2000) Exogenous isolation of antibiotic resistance plasmids from piggery manure slurries reveals a high prevalence and diversity of IncQ-like plasmids. Appl Environ Microbiol 66:4854–4864

    Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Google Scholar 

  • Smit E, Leeflang P, Wernars K (1997) Detection of shifts in microbial community structure and diversity in soil caused by copper contamination using amplified ribosomal DNA restriction analysis. FEMS Microbiol Ecol 23:249–261

    Article  CAS  Google Scholar 

  • Stach JE, Bathe S, Clapp JP, Burns RG (2001) PCR-SSCP comparison of 16S rDNA sequence diversity in soil DNA obtained using different isolation and purification methods. FEMS Microbiol Ecol 36:139–151

    Article  CAS  PubMed  Google Scholar 

  • Stahl DA, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 205–248

    Google Scholar 

  • Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346

    Article  CAS  PubMed  Google Scholar 

  • Stuart GJ, Carlson CA (1986) The biology of natural transformation. Annu Rev Microbiol 40:211–235

    Article  PubMed  Google Scholar 

  • Suzuki MT, Giovannoni SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62:625–630

    CAS  PubMed  Google Scholar 

  • Thomas CM, Smalla K (2000) Trawling the horizontal gene pool. Microbiol Today 27:24–27

    Google Scholar 

  • Thomashow LS, Weller DM (1995) Current concepts in the use of introduced bacteria for biological disease control: mechanisms and antifungal metabolites. In: Stacey G, Keen N (eds) Plant–microbe interactions, vol 1. Chapman & Hall, New York, pp 187–235

    Google Scholar 

  • Thorseth IH, Torsvik T, Torsvik VL, Daae FL, Pedersen R-B, Keldysh -98 Scientific party (2001) Diversity of life in ocean floor basalt. Earth Planet Sci Lett 194:31–37

    Article  CAS  Google Scholar 

  • Tiedje JM, Cho JC, Murray A, Treves D, Xia B, Zhou J (2001) Soil teeming with life: new frontiers for soil science. In: Rees RM, Ball BC, Campbell CD, Watson CA (eds) Sustainable management of soil organic matter. CAB, Wallingford, pp 393–412

    Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Torsvik VL (1980) Isolation of bacterial DNA from soil. Soil Biol Biochem 12:15–22

    Article  CAS  Google Scholar 

  • Torsvik V (1995) Cell extraction method. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer, Dordrecht, pp 1–15

    Google Scholar 

  • Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    Google Scholar 

  • Torsvik V, Daae FL, Goksøyr J (1995) Extraction, purification, and analysis of DNA from soil bacteria. In: Trevors JT, van Elsas JD (eds) Nucleic acids in the environment: methods and applications. Springer, Berlin Heidelberg New York, pp 29–48

    Google Scholar 

  • Torsvik V, Sørheim R, Goksoyr J (1996) Total bacterial diversity in soil and sediment communities—a review. J Ind Microbiol 17:170–178

    Google Scholar 

  • Torsvik V, Daae FL, Sandaa R-A, Øvreås L (2000) Molecular biology and genetic diversity of microorganisms. In: Seckbach J (ed) Journey to diverse microbial worlds. Kluwer, Dordrecht, pp 43–57

    Google Scholar 

  • Torsvik V, Øvreås L, Thingstad TF (2002) Prokaryotic diversity-magnitude, dynamics and controlling factors. Science 296:1064–1066

    Google Scholar 

  • Tschäpe H (1994) The spread of plasmids as a function of bacterial adaptability. FEMS Microbiol Ecol 15:23–32

    Article  Google Scholar 

  • Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936

    Article  CAS  Google Scholar 

  • Van Elsas JD, Smalla K (1996) Methods for sampling soil microbes. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology. ASM, Washington, D.C., pp 383–390

    Google Scholar 

  • Van Elsas JD, Smalla K, Tebbe CC (2000) Extraction and analysis of microbial community nucleic acids from environmental matrices. In: Jansson JK, van Elsas JD, Bailey MJ (eds) Tracking genetically-engineered microorganisms. Eurekah, Austin, Tex., pp 29–51

    Google Scholar 

  • Van Veen JA, Van Overbeck LS, Van Elsas JD (1997) Fate and activity of microorganisms into soil. Mol Biol Rev 61:121–133

    PubMed  Google Scholar 

  • Viebahn M, Glandorf DCM, Ouwens TWM, Smit E, Leeflang P, Wernars K, Thomashow LS, van Loon LC, Bakker PAHM (2003) Repeated introduction of genetically modified Pseudomonas putida WCS358r without intensified effects on the indigenous microflora of field-grown wheat. Appl Environ Microbiol 69:3110–3118

    Google Scholar 

  • Wagner M, Horn M, Daims H (2003) Fluorescence in situ hybridisation for the identification and characterisation of prokaryotes. Curr Opin Microbiol 6:302–309

    Google Scholar 

  • Wardle DA, Giller KE (1996) The quest for a contemporary ecological dimension to soil biology. Soil Biol Biochem 28:1549–1554

    Article  CAS  Google Scholar 

  • Westover KM, Kennedy AC, Kelleys SE (1997) Patterns of rhizosphere microbial community structure associated with co-occurring plant species. J Ecol 85:863–873

    Google Scholar 

  • Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251

    Google Scholar 

  • Widmer F, Seidler RJ, Watrud LS (1996) Sensitive detection of transgenic plant marker gene persistence in soil microcosms. Mol Ecol 5:603–613

    CAS  Google Scholar 

  • Widmer F, Seidler RJ, Donegan KK, Reed GL (1997) Quantification of transgenic plant marker gene persistence in the field. Mol Ecol 6:1–7

    Article  CAS  Google Scholar 

  • Wintzingerode FV, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pit falls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  PubMed  Google Scholar 

  • Witte W (1998) Medical consequences of antibiotic use in agriculture. Science 279:996–997

    Google Scholar 

  • Woese CR (1998) Default taxonomy: Ernst Mayr’s view of the microbial world. Proc Natl Acad Sci 95:11043–11046

    Article  CAS  PubMed  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci 87:4576–4579

    CAS  PubMed  Google Scholar 

  • Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci 96:1463–1468

    Article  CAS  PubMed  Google Scholar 

  • Yan A, McBratney B, Copeland L (2000) Functional substrate biodiversity of cultivated and uncultivated A horizons of vertisols in NW New South Wales. Geoderma 96:321–343

    Article  Google Scholar 

  • Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108

    Article  Google Scholar 

  • Zichichi A (1993) Scienza ed Emergenze Planetarie. Rizzoli, Rome

    Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the support of COST Action 831 for supporting the attendance of authors to the Erice (Trapani, Italy) meeting in 2001. Some of the data presented and discussed in this review by A. Benedetti and P. Nannipieri have been obtained in the research MISA project financed by the Ministero delle Politiche Agericole e Forestali, Italy.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to J. M. Lynch or P. Nannipieri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lynch, J.M., Benedetti, A., Insam, H. et al. Microbial diversity in soil: ecological theories, the contribution of molecular techniques and the impact of transgenic plants and transgenic microorganisms. Biol Fertil Soils 40, 363–385 (2004). https://doi.org/10.1007/s00374-004-0784-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-004-0784-9

Keywords

Navigation