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

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.

[1]  S. Levy.  Antibiotic resistance: an ecological imbalance. , 2007, Ciba Foundation symposium.

[2]  A. Pühler,et al.  Phenotypic and molecular characterization of conjugative antibiotic resistance plasmids isolated from bacterial communities of activated sludge , 2000, Molecular and General Genetics MGG.

[3]  H. Insam,et al.  Impact of heavy metals on the degradative capabilities of soil bacterial communities , 1993, Biology and Fertility of Soils.

[4]  R. Sandaa,et al.  Abundance and Diversity of Archaea in Heavy-Metal-Contaminated Soils , 1999, Applied and Environmental Microbiology.

[5]  T. Vogel,et al.  Degradation and Transformability of DNA from Transgenic Leaves , 2003, Applied and Environmental Microbiology.

[6]  G. D. Di Giovanni,et al.  Comparison of Parental and Transgenic Alfalfa Rhizosphere Bacterial Communities Using Biolog GN Metabolic Fingerprinting and Enterobacterial Repetitive Intergenic Consensus Sequence-PCR (ERIC-PCR) , 1999, Microbial Ecology.

[7]  N. Pace,et al.  Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Saxena,et al.  Insecticidal toxin from Bacillus thuringiensis is released from roots of transgenic Bt corn in vitro and in situ. , 2000, FEMS microbiology ecology.

[9]  V. Torsvik.  Cell extraction method. , 1995 .

[10]  J. Clapp,et al.  PCR-SSCP comparison of 16S rDNA sequence diversity in soil DNA obtained using different isolation and purification methods. , 2001, FEMS microbiology ecology.

[11]  G. Kowalchuk,et al.  Detection and characterization of fungal infections of Ammophila arenaria (marram grass) roots by denaturing gradient gel electrophoresis of specifically amplified 18s rDNA , 1997, Applied and environmental microbiology.

[12]  J. Borneman,et al.  Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation , 1997, Applied and environmental microbiology.

[13]  K. Giller,et al.  Long-term effects of metals in sewage sludge on soils, microorganisms and plants , 1995, Journal of Industrial Microbiology.

[14]  Rolf B. Pedersen,et al.  Diversity of life in ocean floor basalt , 2001 .

[15]  Michael Wagner,et al.  Fluorescence in situ hybridisation for the identification and characterisation of prokaryotes. , 2003, Current opinion in microbiology.

[16]  P. Simonet,et al.  Natural Transformation of Pseudomonas fluorescens and Agrobacterium tumefaciens in Soil , 2001, Applied and Environmental Microbiology.

[17]  P. Oger,et al.  Effect of crop rotation and soil cover on alteration of the soil microflora generated by the culture of transgenic plants producing opines , 2000, Molecular ecology.

[18]  T. Vogel,et al.  Laboratory-Scale Evidence for Lightning-Mediated Gene Transfer in Soil , 2001, Applied and Environmental Microbiology.

[19]  K. Nielsen,et al.  Transformation of Acinetobacter sp. Strain BD413(pFG4ΔnptII) with Transgenic Plant DNA in Soil Microcosms and Effects of Kanamycin on Selection of Transformants , 2000, Applied and Environmental Microbiology.

[20]  Michael Wagner,et al.  probeBase: an online resource for rRNA-targeted oligonucleotide probes , 2003, Nucleic Acids Res..

[21]  K. Mullis,et al.  Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. , 1985, Science.

[22]  J. Prosser,et al.  Bacterial Origin and Community Composition in the Barley Phytosphere as a Function of Habitat and Presowing Conditions , 2000, Applied and Environmental Microbiology.

[23]  W. Wackernagel,et al.  Establishment of introduced antagonistic bacteria in the rhizosphere of transgenic potatoes and their effect on the bacterial community. , 2000, FEMS microbiology ecology.

[24]  J. V. van Elsas,et al.  Molecular Method To Assess the Diversity of Burkholderia Species in Environmental Samples , 2002, Applied and Environmental Microbiology.

[25]  J. Hutton,et al.  Thermal stability and renaturation of DNA in dimethyl sulfoxide solutions: Acceleration of the renaturation rate , 1980, Biopolymers.

[26]  J. D. Elsas,et al.  Methods for Sampling of Soil Microbes , 1996 .

[27]  P. Nannipieri,et al.  Microbial diversity and soil functions , 2003 .

[28]  J. V. van Elsas,et al.  Assessment of bacterial community structure in soil by polymerase chain reaction and denaturing gradient gel electrophoresis. , 1999, Journal of microbiological methods.

[29]  Rudolf Amann,et al.  Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria , 2002, Applied and Environmental Microbiology.

[30]  B. Griffiths,et al.  Analysis of soil and bacterioplankton community DNA by melting profiles and reassociation kinetics , 1997 .

[31]  D. Harris.  Analyses of DNA extracted from microbial communities , 1994 .

[32]  U. Göbel,et al.  Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. , 1997, FEMS microbiology reviews.

[33]  W. Witte,et al.  Medical Consequences of Antibiotic Use in Agriculture , 1998, Science.

[34]  Wilfried Wackernagel,et al.  Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  K. Schleifer,et al.  Detection of micro-organisms in soil after in situ hybridization with rRNA-targeted, fluorescently labelled oligonucleotides. , 1992, Journal of general microbiology.

[36]  H. Heuer,et al.  Influence of transgenic T4-lysozyme-producing potato plants on potentially beneficial plant-associated bacteria , 1999 .

[37]  J. Hantula,et al.  Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA , 2000 .

[38]  H. Heuer,et al.  Bulk and Rhizosphere Soil Bacterial Communities Studied by Denaturing Gradient Gel Electrophoresis: Plant-Dependent Enrichment and Seasonal Shifts Revealed , 2001, Applied and Environmental Microbiology.

[39]  J. V. van Elsas,et al.  Application of a novel Paenibacillus-specific PCR-DGGE method and sequence analysis to assess the diversity of Paenibacillus spp. in the maize rhizosphere. , 2003, Journal of microbiological methods.

[40]  K. Nielsen,et al.  Evaluation of possible horizontal gene transfer from transgenic plants to the soil bacterium Acinetobacter calcoaceticus BD413 , 1997, Theoretical and Applied Genetics.

[41]  K. Nielsen,et al.  Induced Natural Transformation of Acinetobacter calcoaceticus in Soil Microcosms , 1997, Applied and environmental microbiology.

[42]  W. Liesack,et al.  Occurrence of novel groups of the domain Bacteria as revealed by analysis of genetic material isolated from an Australian terrestrial environment , 1992, Journal of bacteriology.

[43]  A. C. Kennedy,et al.  Patterns of Rhizosphere Microbial Community Structure Associated with Co-Occurring Plant Species , 1997 .

[44]  R. Dick,et al.  Enzymes in the environment , 2002 .

[45]  A. Massol-Deyá,et al.  Bacterial community fingerprinting of amplified 16S and 16–23S ribosomal DNA gene sequences and restriction endonuclease analysis(ARDRA) , 1995 .

[46]  K. Smalla,et al.  Transformation of Acinetobacter sp. Strain BD413 by Transgenic Sugar Beet DNA , 1998, Applied and Environmental Microbiology.

[47]  W. Wackernagel,et al.  Increased Killing of Bacillus subtilison the Hair Roots of Transgenic T4 Lysozyme-Producing Potatoes , 2000, Applied and Environmental Microbiology.

[48]  J. Weiner,et al.  Fundamentals and applications , 2003 .

[49]  D. Lane.  16S/23S rRNA sequencing , 1991 .

[50]  R. Rees,et al.  Sustainable Management of Soil Organic Matter , 2000 .

[51]  B. Schierwater,et al.  Applications of random amplified polymorphic DNA (RAPD) in molecular ecology , 1992, Molecular ecology.

[52]  F. O'Gara,et al.  Isolation of 2,4-Diacetylphloroglucinol from a Fluorescent Pseudomonad and Investigation of Physiological Parameters Influencing Its Production , 1992, Applied and environmental microbiology.

[53]  L. Øvreås,et al.  Microbial Diversity and Community Structure in Two Different Agricultural Soil Communities , 1998, Microbial Ecology.

[54]  L. Overbeek,et al.  Fate and activity of microorganisms introduced into soil. , 1997 .

[55]  H. Heuer,et al.  Effects of T4 Lysozyme Release from Transgenic Potato Roots on Bacterial Rhizosphere Communities Are Negligible Relative to Natural Factors , 2002, Applied and Environmental Microbiology.

[56]  A. Mead,et al.  Control of Allium white rot (Sclerotium cepivorum) with composted onion waste , 2002 .

[57]  L. Øvreås,et al.  Prokaryotic Diversity--Magnitude, Dynamics, and Controlling Factors , 2002, Science.

[58]  Kornelia Smalla,et al.  Exogenous Isolation of Antibiotic Resistance Plasmids from Piggery Manure Slurries Reveals a High Prevalence and Diversity of IncQ-Like Plasmids , 2000, Applied and Environmental Microbiology.

[59]  V. Torsvik,et al.  Bacterial and fungal activities in soil: Separation of bacteria and fungi by a rapid fractionated centrifugation technique , 1977 .

[60]  K. Smalla,et al.  Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer , 1999 .

[61]  L. Forney,et al.  Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA , 1997, Applied and environmental microbiology.

[62]  Y. Zo,et al.  Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand-conformation polymorphism , 1996, Applied and environmental microbiology.

[63]  D. Chadwick,et al.  Antibiotic resistance : origins, evolution, selection, and spread , 1997 .

[64]  E. Stackebrandt,et al.  Automated fragment length analysis of fluorescently-labeled 16S rDNA after digestion with 4-base cutting restriction enzymes , 1998 .

[65]  W. Holben,et al.  DNA‐based monitoring of total bacterial community structure in environmental samples , 1995, Molecular ecology.

[66]  R. Tate.  Microbial Communities, Functional versus Structural Approaches , 1998 .

[67]  F. O'Gara,et al.  An integrated approach for the evaluation of biological control of the complex Polymyxa betae/Beet Necrotic Yellow Vein Virus, by means of seed inoculants , 2001, Plant and Soil.

[68]  S. Siciliano,et al.  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 , 1999 .

[69]  W. Liesack,et al.  Detection of Methanotroph Diversity on Roots of Submerged Rice Plants by Molecular Retrieval ofpmoA, mmoX, mxaF, and 16S rRNA and Ribosomal DNA, Including pmoA-Based Terminal Restriction Fragment Length Polymorphism Profiling , 2001, Applied and Environmental Microbiology.

[70]  J. P. Grime,et al.  Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges , 2001, Science.

[71]  L. Thomashow,et al.  Current Concepts in the Use of Introduced Bacteria for Biological Disease Control: Mechanisms and Antifungal Metabolites , 1996 .

[72]  X. Nesme,et al.  Conditions for natural transformation of Ralstonia solanacearum , 1997, Applied and environmental microbiology.

[73]  L. Ranjard,et al.  Sequencing Bands of Ribosomal Intergenic Spacer Analysis Fingerprints for Characterization and Microscale Distribution of Soil Bacterium Populations Responding to Mercury Spiking , 2000, Applied and Environmental Microbiology.

[74]  Ken E. Giller,et al.  Agricultural intensification, soil biodiversity and agroecosystem function , 1997 .

[75]  H. Heuer,et al.  Polynucleotide Probes That Target a Hypervariable Region of 16S rRNA Genes To Identify Bacterial Isolates Corresponding to Bands of Community Fingerprints , 1999, Applied and Environmental Microbiology.

[76]  C. Kuske,et al.  Assessment of Microbial Diversity in Four Southwestern United States Soils by 16S rRNA Gene Terminal Restriction Fragment Analysis , 2000, Applied and Environmental Microbiology.

[77]  A. Squartini,et al.  Fate of genetically modified Rhizobium leguminosarum biovar viciae during long-term storage of commercial inoculants. , 1996, The Journal of applied bacteriology.

[78]  P. Saxman,et al.  Terminal Restriction Fragment Length Polymorphism Analysis Program, a Web-Based Research Tool for Microbial Community Analysis , 2000, Applied and Environmental Microbiology.

[79]  K. Bruce,et al.  Analysis of mer Gene Subclasses within Bacterial Communities in Soils and Sediments Resolved by Fluorescent-PCR-Restriction Fragment Length Polymorphism Profiling , 1997, Applied and environmental microbiology.

[80]  C. Carlson,et al.  The biology of natural transformation. , 1986, Annual review of microbiology.

[81]  R. Pukall,et al.  Prevalence of nptII and Tn5 in kanamycin‐resistant bacteria from different environments , 1993 .

[82]  C. Brunk,et al.  A molecular technique for identification of bacteria using small subunit ribosomal RNA sequences. , 1994, BioTechniques.

[83]  L. Watrud,et al.  Sensitive detection of transgenic plant marker gene persistence in soil microcosms , 1996 .

[84]  E. Stackebrandt,et al.  Nucleic acid techniques in bacterial systematics , 1991 .

[85]  F. D. de Bruijn,et al.  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 , 1992, Applied and environmental microbiology.

[86]  E. Triplett,et al.  Automated Approach for Ribosomal Intergenic Spacer Analysis of Microbial Diversity and Its Application to Freshwater Bacterial Communities , 1999, Applied and Environmental Microbiology.

[87]  J. Jansson.  Tracking Genetically-Engineered Microorganisms , 2000 .

[88]  H. Heuer,et al.  Analysis of BIOLOG GN Substrate Utilization Patterns by Microbial Communities , 1998, Applied and Environmental Microbiology.

[89]  S. McNaughton,et al.  Diversity and stability , 1988, Nature.

[90]  S. Hall,et al.  Biodiversity-productivity relations: an experimental evaluation of mechanisms , 2000, Oecologia.

[91]  J. Handelsman,et al.  Toward functional genomics in bacteria: analysis of gene expression in Escherichia coli from a bacterial artificial chromosome library of Bacillus cereus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[92]  R. Costa,et al.  Dynamics of Fungal Communities in Bulk and Maize Rhizosphere Soil in the Tropics , 2003, Applied and Environmental Microbiology.

[93]  F. O'Gara,et al.  Environmental impact of genetically modified Azospirillum brasilense, Pseudomonas fluorescens, and Rhizobium leguminosarum released as soil/seed inoculants , 1994 .

[94]  W. Wackernagel,et al.  Spread of Recombinant DNA by Roots and Pollen of Transgenic Potato Plants, Identified by Highly Specific Biomonitoring Using Natural Transformation of an Acinetobacter sp , 2003, Applied and Environmental Microbiology.

[95]  Hartmann,et al.  16S rDNA analysis for characterization of denitrifying bacteria isolated from three agricultural soils. , 2000, FEMS microbiology ecology.

[96]  H. Insam,et al.  Microbial Community Dynamics During Composting of Organic Matter as Determined by 16S Ribosomal DNA Analysis , 2002 .

[97]  D. Chadwick,et al.  Ciba Foundation Symposium 207 - Antibiotic Resistance: Origins, Evolution, Selection and Spread , 1997 .

[98]  David A. Stahl,et al.  Development and application of nucleic acid probes , 1991 .

[99]  B. Degens,et al.  Development of a physiological approach to measuring the catabolic diversity of soil microbial communities , 1997 .

[100]  R. Rees,et al.  Soil teeming with life: new frontiers for soil science. , 2001 .

[101]  J. T. Staley,et al.  Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. , 1985, Annual review of microbiology.

[102]  K. Schleifer,et al.  Phylogenetic Oligodeoxynucleotide Probes for the Major Subclasses of Proteobacteria: Problems and Solutions , 1992 .

[103]  H. Heuer,et al.  Application of denaturing gradient gel electrophoresis and temperature gradient gel electrophoresis for studying soil microbial communities. , 1997 .

[104]  Hans H. Cheng,et al.  Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA , 1997, Applied and environmental microbiology.

[105]  E. Smit,et al.  Detection of shifts in microbial community structure and diversity in soil caused by copper contamination using amplified ribosomal DNA restriction analysis , 1997 .

[106]  Henry A. Erlich,et al.  Enzymatic amplification of ?-globin genomic sequences and restriction site analysis for diagnosis of , 1985 .

[107]  W. Dzik,et al.  Assays for heparin‐induced thrombocytopenia , 1997, Transfusion medicine.

[108]  A. Wiseman,et al.  Environmental Biomonitoring: The Biotechnology Ecotoxicology Interface , 1998 .

[109]  Julie E. Jones,et al.  Interactions between crop residue and soil organic matter quality and the functional diversity of soil microbial communities , 2002 .

[110]  I. Potrykus,et al.  “Horizontal” Gene Transfer from a Transgenic Potato Line to a Bacterial Pathogen (Erwinia chrysanthemi) Occurs—if at All—at an Extremely Low Frequency , 1995, Bio/Technology.

[111]  R. Sandaa,et al.  Molecular Biology and Genetic Diversity of Microorganisms , 2000 .

[112]  Franziska Schwarz,et al.  Antibiotic resistance spread in food , 1997, Nature.

[113]  K. Nielsen,et al.  Natural transformation and availability of transforming DNA to Acinetobacter calcoaceticus in soil microcosms , 1997, Applied and environmental microbiology.

[114]  H. Insam.  Developments in soil microbiology since the mid 1960s , 2001 .

[115]  C. Tebbe,et al.  Bacterial community composition in the rhizosphere of a transgenic, herbicide-resistant maize (Zea mays) and comparison to its non-transgenic cultivar Bosphore. , 2002, FEMS microbiology ecology.

[116]  J. Borneman,et al.  Molecular microbial diversity of an agricultural soil in Wisconsin , 1996, Applied and environmental microbiology.

[117]  V. Torsvik,et al.  Pesticide effects on bacterial diversity in agricultural soils – a review , 2001, Biology and Fertility of Soils.

[118]  X. Nesme,et al.  During infection of its host, the plant pathogen Ralstonia solanacearum naturally develops a state of competence and exchanges genetic material , 1999 .

[119]  G. Stacey,et al.  Plant-Microbe Interactions , 1996, Plant-Microbe Interactions.

[120]  C. Woese.  Default taxonomy: Ernst Mayr's view of the microbial world. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[121]  C. Keel,et al.  Suppression of root diseases by Pseudomonas fluorescens CHA0 - importance of the bacterial seconday metabolite 2,4-diacetylphloroglucinol , 1992 .

[122]  D. Stahl,et al.  Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens , 1994, Applied and environmental microbiology.

[123]  J. Handelsman,et al.  Cloning the Soil Metagenome: a Strategy for Accessing the Genetic and Functional Diversity of Uncultured Microorganisms , 2000, Applied and Environmental Microbiology.

[124]  M. G. Lorenz,et al.  Natural genetic transformation of Pseudomonas stutzeri in a non-sterile soil. , 1998, Microbiology.

[125]  M. G. Lorenz,et al.  Bacterial gene transfer by natural genetic transformation in the environment. , 1994, Microbiological reviews.

[126]  D. Wardle,et al.  The quest for a contemporary ecological dimension to soil biology , 1996 .

[127]  V. Torsvik.  Isolation of bacterial DNA from soil. , 1980 .

[128]  W. Wackernagel,et al.  The Bacteriolytic Activity in Transgenic Potatoes Expressing a Chimeric T4 Lysozyme Gene and the Effect of T4 Lysozyme on Soil- and Phytopathogenic Bacteria , 1999 .

[129]  E. Top,et al.  Effect of mercury addition on plasmid incidence and gene mobilizing capacity in bulk soil , 1998 .

[130]  A. Mills,et al.  Classification and Characterization of Heterotrophic Microbial Communities on the Basis of Patterns of Community-Level Sole-Carbon-Source Utilization , 1991, Applied and environmental microbiology.

[131]  M. Madigan,et al.  Brock Biology of Microorganisms , 1996 .

[132]  G. Kowalchuk,et al.  Assessing responses of soil microorganisms to GM plants , 2003 .

[133]  H. Heuer,et al.  Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis , 2004, Plant and Soil.

[134]  V. Torsvik,et al.  Total bacterial diversity in soil and sediment communities—A review , 1996, Journal of Industrial Microbiology.

[135]  R Amann,et al.  Analysis of broad-scale differences in microbial community composition of two pristine forest soils. , 1998, Systematic and applied microbiology.

[136]  J. Tiedje,et al.  Characterization of the Dominant and Rare Members of a Young Hawaiian Soil Bacterial Community with Small-Subunit Ribosomal DNA Amplified from DNA Fractionated on the Basis of Its Guanine and Cytosine Composition , 1998, Applied and Environmental Microbiology.

[137]  J. Lynch,et al.  Resilience of the rhizosphere to anthropogenic disturbance , 2004, Biodegradation.

[138]  A. Sessitsch,et al.  Diversity and community structure of culturable Bacillus spp. populations in the rhizospheres of transgenic potatoes expressing the lytic peptide cecropin B , 2003 .

[139]  H. Heuer,et al.  Gentamicin resistance genes in environmental bacteria: prevalence and transfer. , 2002, FEMS microbiology ecology.

[140]  K. Nielsen,et al.  Horizontal gene transfer from transgenic plants to terrestrial bacteria--a rare event? , 1998, FEMS microbiology reviews.

[141]  D. Tilman.  Resource competition and community structure. , 1983, Monographs in population biology.

[142]  R. Whittaker.  Evolution and measurement of species diversity , 1972 .

[143]  R. Vogel,et al.  Diversity of lactic acid bacteria associated with ducks. , 1998, Systematic and applied microbiology.

[144]  E. Odum.  The strategy of ecosystem development. , 1969, Science.

[145]  C. James.  Global Review of Commercialized Transgenic Crops : 1998 , 1999 .

[146]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[147]  G. Kowalchuk,et al.  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 , 2001, Applied and Environmental Microbiology.

[148]  L. Øvreås,et al.  Phenotypic diversity and antibiotic resistance in soil bacterial communities , 1996, Journal of Industrial Microbiology.

[149]  Philippot,et al.  The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type. , 1999, FEMS microbiology ecology.

[150]  R. May,et al.  Stability and Complexity in Model Ecosystems , 1976, IEEE Transactions on Systems, Man, and Cybernetics.

[151]  Jo Handelsman,et al.  Isolation of Antibiotics Turbomycin A and B from a Metagenomic Library of Soil Microbial DNA , 2002, Applied and Environmental Microbiology.

[152]  J. Thioulouse,et al.  Characterization of Bacterial and Fungal Soil Communities by Automated Ribosomal Intergenic Spacer Analysis Fingerprints: Biological and Methodological Variability , 2001, Applied and Environmental Microbiology.

[153]  Diversity of bacterial communities in the rhizosphere and root interior of field‐grown genetically modified Brassica napus , 2001 .

[154]  H. Tschäpe.  The spread of plasmids as a function of bacterial adaptability , 1994 .

[155]  L. Watrud,et al.  A field study with genetically engineered alfalfa inoculated with recombinant Sinorhizobium meliloti: effects on the soil ecosystem , 1999 .

[156]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[157]  Clive James,et al.  Global review of commercialized transgenic crops , 2003 .

[158]  M. G. Lorenz,et al.  Mechanism of Retarded DNA Degradation and Prokaryotic Origin of DNases in Nonsterile Soils , 1997 .

[159]  R. Sandaa,et al.  Influence of long-term heavy-metal contamination on microbial communities in soil , 2001 .

[160]  H. Insam,et al.  Microbial communities : functional versus structural approaches , 1997 .

[161]  Robert M. May,et al.  Theoretical Ecology: Principles and Applications , 1981 .

[162]  P. Simonet,et al.  Horizontal gene transfers in the environment: natural transformation as a putative process for gene transfers between transgenic plants and microorganisms. , 1999, Research in microbiology.

[163]  R. Seidler,et al.  Quantification of transgenic plant marker gene persistence in the field , 1997 .

[164]  C. Nakatsu,et al.  Soil Community Analysis Using DGGE of 16S rDNA Polymerase Chain Reaction Products , 2000 .

[165]  P. Simonet,et al.  Development of engineered genomic DNA to monitor the natural transformation of Pseudomonas stutzeri in soil-like microcosms , 1997 .

[166]  J. Seckbach.  Journey to Diverse Microbial Worlds , 2000, Cellular Origin and Life in Extreme Habitats.

[167]  S. Giovannoni,et al.  Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR , 1996, Applied and environmental microbiology.

[168]  P. Bakker,et al.  Repeated Introduction of Genetically Modified Pseudomonas putida WCS358r without Intensified Effects on the Indigenous Microflora of Field-Grown Wheat , 2003, Applied and Environmental Microbiology.

[169]  S. Sørensen,et al.  Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship , 2000 .

[170]  A. McBratney,et al.  Functional substrate biodiversity of cultivated and uncultivated A horizons of vertisols in NW New South Wales , 2000 .

[171]  K. Schleifer,et al.  Phylogenetic identification and in situ detection of individual microbial cells without cultivation. , 1995, Microbiological reviews.

[172]  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. , 2001, FEMS microbiology letters.

[173]  K. Timmis,et al.  An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. , 2000, Environmental microbiology.

[174]  P. Garbeva,et al.  Predominant Bacillus spp. in Agricultural Soil under Different Management Regimes Detected via PCR-DGGE , 2003, Microbial Ecology.

[175]  W. Wackernagel,et al.  Detection of nptII (kanamycin resistance) genes in genomes of transgenic plants by marker-rescue transformation , 1998, Molecular and General Genetics MGG.

[176]  Sigmund Jensen,et al.  Microbial Community Changes in a Perturbed Agricultural Soil Investigated by Molecular and Physiological Approaches , 1998, Applied and Environmental Microbiology.

[177]  M. Loreau,et al.  Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[178]  V. Torsvik,et al.  Extraction, Purification, and Analysis of DNA from Soil Bacteria , 1995 .

[179]  G. Muyzer,et al.  Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology , 2004, Antonie van Leeuwenhoek.

[180]  K. Giller,et al.  Beyond the Biomass. , 1995 .

[181]  B. Griffiths,et al.  Relationship between Functional Diversity and Genetic Diversity in Complex Microbial Communities , 1997 .

[182]  L. Ranjard,et al.  Monitoring complex bacterial communities using culture-independent molecular techniques: application to soil environment. , 2000, Research in microbiology.

[183]  Robert M. May,et al.  Theoretical Ecology: Principles and Applications , 1977 .

[184]  J. Dighton,et al.  The role of abiotic factors, cultivation practices and soil fauna in the dispersal of genetically modified microorganisms in soils , 1997 .

[185]  A. Sessitsch,et al.  Effects of transgenic glufosinate-tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. , 2002, FEMS microbiology ecology.

[186]  T. Vamerali,et al.  Field release of genetically marked Azospirillum brasilense in association with Sorghum bicolor L. , 2004, Plant and Soil.

[187]  W. S. Silver.  Microbial ecology. , 1967, Science.

[188]  C. Tebbe,et al.  A New Approach To Utilize PCR–Single-Strand-Conformation Polymorphism for 16S rRNA Gene-Based Microbial Community Analysis , 1998, Applied and Environmental Microbiology.

[189]  Shobha Sharma,et al.  Different Carbon Source Utilization ProfIles of Four Tropical Soils from Ethiopia , 1997 .

[190]  D A Stahl,et al.  Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology , 1990, Journal of bacteriology.

[191]  R. Macarthur.  Fluctuations of Animal Populations and a Measure of Community Stability , 1955 .

[192]  J. D. Elsas,et al.  Extraction and analysis of microbial community nucleic acids from environmental matrices , 2000 .

[193]  J. D. Elsas,et al.  Molecular Microbial Ecology Manual , 2013, Springer Netherlands.

[194]  R. Atlas,et al.  Microbial Ecology: Fundamentals and Applications. , 1982 .

[195]  A. Fox,et al.  Utility of 16S–23S rRNA spacer region methodology: how similar are interspace regions within a genome and between strains for closely related organisms? , 1998 .

[196]  M. Willig,et al.  Functional diversity of microbial communities: A quantitative approach , 1994 .

[197]  P. Simonet,et al.  On the track of natural transformation in soil , 1994 .

[198]  M. Bailey,et al.  Effect of Insertion Site and Metabolic Load on the Environmental Fitness of a Genetically Modified Pseudomonas fluorescensIsolate , 1998, Applied and Environmental Microbiology.

[199]  S. Perotto,et al.  The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility , 2002, Biology and Fertility of Soils.

[200]  R. Fani,et al.  Transformation of Bacillus subtilis by DNA bound on clay in non-sterile soil. , 1994 .

[201]  Hahn,et al.  Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. , 1999, FEMS microbiology ecology.

[202]  H. Heuer,et al.  Evaluation of community-level catabolic profiling using BIOLOG GN microplates to study microbial community changes in potato phyllosphere , 1997 .

[203]  V. Torsvik,et al.  High diversity in DNA of soil bacteria , 1990, Applied and environmental microbiology.

[204]  O. Kandler,et al.  Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[205]  R. Ohtonen,et al.  Ecological theories in soil biology , 1997 .