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.
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
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
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
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
Atlas RM, Bartha R (1998) Microbial ecology. Fundamentals and applications, 4th edn. Addison-Wesley, Reading
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
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
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
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
Bertolla F, van Gijsegem F, Nesmer X, Simonet P (1997) Conditions for natural transformation of Ralstonia solanacearum. Appl Environ Microbiol 63:4965–4968
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Escara JF, Hutton JR (1980) Thermal stability and renaturation of DNA in dimethyl sulfoxide solutions: acceleration of the renaturation rate. Biopolymers 19:1315–1327
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
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
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
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
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
Gebhard F, Smalla K (1998) Transformation of Acinetobacter sp. strain BD413 by transgenic sugar beet DNA. Appl Environ Microbiol 64:1550–1554
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
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
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
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
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
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
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
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
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
Hadrys H, Balick M, Schierwater B (1992) Applications of random amplified polymorphic DNA (RAPD) in molecular ecology. Mol Ecol 1:55–63
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
Hall SJ, Gray SA, Hammett ZL (2000) Biodiversity-productivity relations: an experimental evaluation of mechanisms. Oecologia 122:545–555
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
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
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
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
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
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
Holben WE, Harris D (1995) DNA-based monitoring of total bacterial community structure in environmental samples. Mol Ecol 4:627–631
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
Insam H (2001) Development in soil microbiology since mid 1960s. Geoderma 100:389–402
James C (2003) Global review of commercialized transgenic crops: 2002. ISAA Briefs 29:3–38
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
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
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
Kowalchuk GA, Bruinsma M, van Veen JA (2003) Assessing responses of soil microorganisms to GM plants. Trends Ecol Evol 18:403–410
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175
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
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
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
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
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
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
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
Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602
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
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
Loy A, Horn M, Wagner M (2003) probeBase—an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res 31:514–516
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
MacArthur RH (1955) Fluctuations of animal populations, and a measure of stability. Ecology 36:533–536
Madigan MT, Martinko JM, Parker J (2003) Brock biology of microorganisms, 10th edn. Pearson Education, Prentice Hall, Upper Saddle River, Toronto
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
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
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
May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, Princeton, N.J.
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
McNaughton SJ (1988) Diversity and stability. Nature 333:204–205
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
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
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
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
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
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
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
Nielsen KM, Bones AM, van Elsas JD (1997b) Induced natural transformation of Acinetobacter calcoaceticus in soil microcosms. Appl Environ Microbiol 63:3972–3977
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
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
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
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
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
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
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
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
Odum EP (1969) The strategy of ecosystem development. Science 164:262–270
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
Ohtonen R, Aikio S, Vare H (1997) Ecological theories in soil biology. Soil Biol Biochem 29:1613–1619
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
Øvreås L, Torsvik V (1998) Microbial diversity and community structure in two different agricultural soil communities. Microb Ecol 36:306–315
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
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
Paget E, Simonet P (1994) On the track of natural transformation in soil. FEMS Microbiol Ecol 15:109–118
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
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
Perreten V, Schwarz F, Cresta L, Boeglin M, Dasen G, Teuber M (1997) Antibiotic resistance spread in food. Nature 389:801–802
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
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
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
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
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
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
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
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
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
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
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
Salyers A (1996) The real threat from antibiotics. Nature 384:304
Sandaa R-A, Enger Ø, Torsvik V (1999a) Abundance and diversity of Archaea in heavy-metal contaminated soils. Appl Environ Microbiol 65:3293–3297
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
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
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
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
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
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
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
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
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
Shannon CE, Weaver W (1969) The mathematical theory of communication. University of Illinois Press, Urbana, Ill.
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
Sikorski J, Graupner S, Lorenz MG, Wackernagel W (1998) Natural transformation of Pseudomonas stutzeri in a non-sterile soil. Microbiology 144:569–576
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
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
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
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
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
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
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
Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346
Stuart GJ, Carlson CA (1986) The biology of natural transformation. Annu Rev Microbiol 40:211–235
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
Thomas CM, Smalla K (2000) Trawling the horizontal gene pool. Microbiol Today 27:24–27
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
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
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
Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, N.J.
Torsvik VL (1980) Isolation of bacterial DNA from soil. Soil Biol Biochem 12:15–22
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
Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787
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
Torsvik V, Sørheim R, Goksoyr J (1996) Total bacterial diversity in soil and sediment communities—a review. J Ind Microbiol 17:170–178
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
Torsvik V, Øvreås L, Thingstad TF (2002) Prokaryotic diversity-magnitude, dynamics and controlling factors. Science 296:1064–1066
Tschäpe H (1994) The spread of plasmids as a function of bacterial adaptability. FEMS Microbiol Ecol 15:23–32
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
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
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
Van Veen JA, Van Overbeck LS, Van Elsas JD (1997) Fate and activity of microorganisms into soil. Mol Biol Rev 61:121–133
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
Wagner M, Horn M, Daims H (2003) Fluorescence in situ hybridisation for the identification and characterisation of prokaryotes. Curr Opin Microbiol 6:302–309
Wardle DA, Giller KE (1996) The quest for a contemporary ecological dimension to soil biology. Soil Biol Biochem 28:1549–1554
Westover KM, Kennedy AC, Kelleys SE (1997) Patterns of rhizosphere microbial community structure associated with co-occurring plant species. J Ecol 85:863–873
Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251
Widmer F, Seidler RJ, Watrud LS (1996) Sensitive detection of transgenic plant marker gene persistence in soil microcosms. Mol Ecol 5:603–613
Widmer F, Seidler RJ, Donegan KK, Reed GL (1997) Quantification of transgenic plant marker gene persistence in the field. Mol Ecol 6:1–7
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
Witte W (1998) Medical consequences of antibiotic use in agriculture. Science 279:996–997
Woese CR (1998) Default taxonomy: Ernst Mayr’s view of the microbial world. Proc Natl Acad Sci 95:11043–11046
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
Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci 96:1463–1468
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
Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108
Zichichi A (1993) Scienza ed Emergenze Planetarie. Rizzoli, Rome
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
Corresponding authors
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-004-0784-9