The magic and menace of metagenomics: prospects for the study of plant growth-promoting rhizobacteria

This article aims to be a pragmatic primer into the field of metagenomics with special emphasis on the prospective contributions of metagenomics to the study of plant growth-promoting rhizobacteria (PGPR). After an introduction into the concepts and methodologies of metagenomics and a discussion of the numerous emerging variations on the basic theme, there will follow a short overview of the success stories in metagenomics (the ‘magic’ in the title of this review), a brief discussion about the technical problems and unrealistic expectations that are sometimes associated with metagenomics (the ‘menace’), and a shortlist of the lessons that can be learned by those that wish to explore the utility of metagenomics in the study of PGPR.

[1]  M. Dumont,et al.  Identification of a complete methane monooxygenase operon from soil by combining stable isotope probing and metagenomic analysis. , 2006, Environmental microbiology.

[2]  H. Rodríguez,et al.  Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. , 2000, Journal of biotechnology.

[3]  Marion Leclerc,et al.  Proteorhodopsin phototrophy in the ocean , 2001, Nature.

[4]  W. Vahjen,et al.  Interference of humic acids and DNA extracted directly from soil in detection and transformation of recombinant DNA from bacteria and a yeast , 1993, Applied and environmental microbiology.

[5]  Lior Pachter,et al.  Bioinformatics for Whole-Genome Shotgun Sequencing of Microbial Communities , 2005, PLoS Comput. Biol..

[6]  P. Hugenholtz,et al.  Laboratory Cultivation of Widespread and Previously Uncultured Soil Bacteria , 2003, Applied and Environmental Microbiology.

[7]  Jo Handelsman,et al.  Metagenomics or Megagenomics? , 2005, Nature Reviews Microbiology.

[8]  Ernest Szeto,et al.  Symbiosis insights through metagenomic analysis of a microbial consortium. , 2006, Nature Reviews Microbiology.

[9]  J. Staunton,et al.  Polyketide biosynthesis: a millennium review. , 2001, Natural product reports.

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

[11]  P. Vyas,et al.  Strain improvement of chitinolytic enzyme producing isolate Pantoea dispersa for enhancing its biocontrol potential against fungal plant pathogens , 2004 .

[12]  Youguo Li,et al.  Screening a wide host-range, waste-water metagenomic library in tryptophan auxotrophs of Rhizobium leguminosarum and of Escherichia coli reveals different classes of cloned trp genes. , 2005, Environmental microbiology.

[13]  Wolfgang Liebl,et al.  Direct Cloning from Enrichment Cultures, a Reliable Strategy for Isolation of Complete Operons and Genes from Microbial Consortia , 2001, Applied and Environmental Microbiology.

[14]  Jürgen Eck,et al.  Metagenomics and industrial applications , 2005, Nature Reviews Microbiology.

[15]  G. Gottschalk,et al.  Construction of Environmental DNA Libraries inEscherichia coli and Screening for the Presence of Genes Conferring Utilization of 4-Hydroxybutyrate , 1999, Applied and Environmental Microbiology.

[16]  Pascale Jeannin,et al.  Recombinant Environmental Libraries Provide Access to Microbial Diversity for Drug Discovery from Natural Products , 2003, Applied and Environmental Microbiology.

[17]  M. Friedrich Stable-isotope probing of DNA: insights into the function of uncultivated microorganisms from isotopically labeled metagenomes. , 2006, Current opinion in biotechnology.

[18]  T. Schmidt,et al.  Diversity and dynamics of microbial communities in soils from agro-ecosystems. , 2003, Environmental microbiology.

[19]  B. Glick,et al.  Applications of free living plant growth-promoting rhizobacteria , 2004, Antonie van Leeuwenhoek.

[20]  J. Handelsman,et al.  Genetics of Zwittermicin A Production by Bacillus cereus , 2004, Applied and Environmental Microbiology.

[21]  R. Bostock,et al.  Rapid In Situ Assay for Indoleacetic Acid Production by Bacteria Immobilized on a Nitrocellulose Membrane , 1991, Applied and environmental microbiology.

[22]  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.

[23]  Forest Rohwer,et al.  An application of statistics to comparative metagenomics , 2006, BMC Bioinformatics.

[24]  J. Handelsman,et al.  Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. , 2004, Environmental microbiology.

[25]  G. Kowalchuk,et al.  Molecular microbial ecology manual. Volumes 1 and 2. , 2004 .

[26]  J. Fuhrman,et al.  Extraction from Natural Planktonic Microorganisms of DNA Suitable for Molecular Biological Studies , 1988, Applied and environmental microbiology.

[27]  E. Delong,et al.  Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior , 2006, Science.

[28]  C. Sensen,et al.  First insight into the genome of an uncultivated crenarchaeote from soil. , 2002, Environmental microbiology.

[29]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Bally,et al.  Physical organization of phytobeneficial genes nifH and ipdC in the plant growth-promoting rhizobacterium Azospirillum lipoferum 4VI. , 2005, FEMS microbiology letters.

[31]  Vivian Miao,et al.  Complementation of daptomycin dptA and dptD deletion mutations in trans and production of hybrid lipopeptide antibiotics. , 2006, Microbiology.

[32]  Hideaki Sugawara,et al.  Novel phylogenetic studies of genomic sequence fragments derived from uncultured microbe mixtures in environmental and clinical samples. , 2005, DNA research : an international journal for rapid publication of reports on genes and genomes.

[33]  Daniel Rokhsar,et al.  Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics , 2004, Science.

[34]  L. Saleena,et al.  Biological suppression of rice diseases by Pseudomonas spp. under saline soil conditions , 2003, Plant and Soil.

[35]  Heather K. Allen,et al.  Intracellular Screen To Identify Metagenomic Clones That Induce or Inhibit a Quorum-Sensing Biosensor , 2005, Applied and Environmental Microbiology.

[36]  J. Tiedje,et al.  DNA recovery from soils of diverse composition , 1996, Applied and environmental microbiology.

[37]  M. Moran,et al.  Analysis of Microbial Gene Transcripts in Environmental Samples , 2005, Applied and Environmental Microbiology.

[38]  J. Handelsman,et al.  Metagenomics: genomic analysis of microbial communities. , 2004, Annual review of genetics.

[39]  Dylan Chivian,et al.  Genomics for environmental microbiology. , 2006, Current opinion in biotechnology.

[40]  W. Doolittle,et al.  Lateral gene transfer and phylogenetic assignment of environmental fosmid clones. , 2005, Environmental microbiology.

[41]  D. Juraeva,et al.  Detection and quantification of the nifH gene in shoot and root of cucumber plants. , 2006, Canadian journal of microbiology.

[42]  T. Abe,et al.  Substrate-induced gene-expression screening of environmental metagenome libraries for isolation of catabolic genes , 2005, Nature Biotechnology.

[43]  R. Costa,et al.  Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. , 2006, Environmental microbiology.

[44]  J. Handelsman,et al.  Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. , 1998, Chemistry & biology.

[45]  Mihai Pop,et al.  Microbiome Metagenomic Analysis of the Human Distal Gut , 2009 .

[46]  Rolf Daniel,et al.  Identification and Characterization of Coenzyme B12-Dependent Glycerol Dehydratase- and Diol Dehydratase-Encoding Genes from Metagenomic DNA Libraries Derived from Enrichment Cultures , 2003, Applied and Environmental Microbiology.

[47]  S. Timmuska,et al.  Cytokinin production by Paenibacillus polymyxa , 1999 .

[48]  Yanhe Ma,et al.  Identification of Eukaryotic Open Reading Frames in Metagenomic cDNA Libraries Made from Environmental Samples , 2006, Applied and Environmental Microbiology.

[49]  G. Gottschalk,et al.  Screening of Environmental DNA Libraries for the Presence of Genes Conferring Na+(Li+)/H+Antiporter Activity on Escherichia coli: Characterization of the Recovered Genes and the Corresponding Gene Products , 2001, Journal of bacteriology.

[50]  A. Chatzinotas,et al.  Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. , 2003, Environmental microbiology.

[51]  P. Weisbeek,et al.  A siderophore peptide synthetase gene from plant-growth-promoting Pseudomonas putida WCS358. , 2001, Systematic and applied microbiology.

[52]  J. Leveau,et al.  Genomic flank-sequencing of plasposon insertion sites for rapid identification of functional genes. , 2006, Journal of microbiological methods.

[53]  Timothy B. Stockwell,et al.  The Sequence of the Human Genome , 2001, Science.

[54]  Dick B Janssen,et al.  Quantifying the accessibility of the metagenome by random expression cloning techniques. , 2004, Environmental microbiology.

[55]  K. Ulaganathan,et al.  Antagonism of Bacillus species (strain BC121) towards Curvularia lunata. , 2002 .

[56]  T. Schmidt,et al.  New Strategies for Cultivation and Detection of Previously Uncultured Microbes , 2004, Applied and Environmental Microbiology.

[57]  B. Andresen,et al.  Genomic analysis of uncultured marine viral communities , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[58]  M. Sliwinski,et al.  Comparison of Crenarchaeal Consortia Inhabiting the Rhizosphere of Diverse Terrestrial Plants with Those in Bulk Soil in Native Environments , 2004, Applied and Environmental Microbiology.

[59]  O. White,et al.  Environmental Genome Shotgun Sequencing of the Sargasso Sea , 2004, Science.

[60]  Jürgen Eck,et al.  Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics , 2003, Molecular microbiology.

[61]  Wolfgang R Streit,et al.  Metagenomics--the key to the uncultured microbes. , 2004, Current opinion in microbiology.

[62]  E. Delong,et al.  Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing , 1991, Journal of bacteriology.

[63]  E. Koonin,et al.  Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. , 2000, Environmental microbiology.

[64]  Joern Hopke,et al.  Genetically Modified Bacterial Strains and Novel Bacterial Artificial Chromosome Shuttle Vectors for Constructing Environmental Libraries and Detecting Heterologous Natural Products in Multiple Expression Hosts , 2004, Applied and Environmental Microbiology.

[65]  Rolf Daniel,et al.  Construction and Screening of Metagenomic Libraries Derived from Enrichment Cultures: Generation of a Gene Bank for Genes Conferring Alcohol Oxidoreductase Activity on Escherichia coli , 2003, Applied and Environmental Microbiology.

[66]  S. Chen,et al.  Isolation and identification of nitrogen‐fixing bacilli from plant rhizospheres in Beijing region , 2005, Journal of applied microbiology.

[67]  Jun-ying Jiao,et al.  Enrichment for microbes living in association with plant tissues , 2006, Journal of applied microbiology.

[68]  Werner Liesack,et al.  Genome of Rice Cluster I Archaea—the Key Methane Producers in the Rice Rhizosphere , 2006, Science.

[69]  Z. Omer,et al.  Indole-3-acetic acid production by pink-pigmented facultative methylotrophic bacteria , 2004, Plant Growth Regulation.

[70]  J. Vessey Plant growth promoting rhizobacteria as biofertilizers , 2003, Plant and Soil.

[71]  H. Nakayashiki,et al.  Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. , 2005, Molecular plant-microbe interactions : MPMI.

[72]  G. Kowalchuk,et al.  Purification of microbial genes from soil and rhizosphere by magnetic capture hybridization and subsequent amplification of target genes by PCR. , 2004 .

[73]  J. Banfield,et al.  Community structure and metabolism through reconstruction of microbial genomes from the environment , 2004, Nature.

[74]  B R Glick,et al.  Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. , 1998, Canadian journal of microbiology.

[75]  E. Wellington,et al.  Isolation of high molecular weight DNA from soil for cloning into BAC vectors. , 2003, FEMS microbiology letters.

[76]  B. M. Gardener,et al.  Microbial populations responsible for specific soil suppressiveness to plant pathogens. , 2002, Annual review of phytopathology.

[77]  P. Bakker,et al.  Biocontrol by Phenazine-1-carboxamide-Producing Pseudomonas chlororaphis PCL1391 of Tomato Root Rot Caused by Fusarium oxysporum f. sp. radicis-lycopersici , 1998 .

[78]  D. Janssen,et al.  Construction, characterization, and use of small-insert gene banks of DNA isolated from soil and enrichment cultures for the recovery of novel amidases. , 2004, Environmental microbiology.

[79]  D. Nam,et al.  $Pyoverdin_{2112}$ of Pseudomonas fluorescens 2112 Inhibits Phytophthora capsici, a Red-Pepper Blight-Causing Fungus , 2003 .

[80]  J. Leveau,et al.  Phylogeny-function analysis of (meta)genomic libraries: screening for expression of ribosomal RNA genes by large-insert library fluorescent in situ hybridization (LIL-FISH). , 2004, Environmental microbiology.

[81]  B R Glick,et al.  Genetic manipulation of plant growth-promoting bacteria to enhance biocontrol of phytopathogens. , 1997, Biotechnology advances.

[82]  T. Vogel,et al.  Potential of a 16S rRNA-Based Taxonomic Microarray for Analyzing the Rhizosphere Effects of Maize on Agrobacterium spp. and Bacterial Communities , 2006, Applied and Environmental Microbiology.

[83]  K. Downing,et al.  Introduction of the Serratia marcescens chiA gene into an endophytic Pseudomonas fluorescens for the biocontrol of phytopathogenic fungi. , 2000, Canadian journal of microbiology.

[84]  M. Marahiel,et al.  Isolation and characterization of a transposon mutant of Pseudomonas fluorescens AU63 deficient in antifungal activity against Pythium ultimum N. Rajendran , 1998 .

[85]  M. Wagner,et al.  The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. , 2006, Current opinion in biotechnology.

[86]  R. Costa,et al.  Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. , 2006, FEMS microbiology ecology.

[87]  Y. Hashidoko,et al.  Soft Gel Medium Solidified with Gellan Gum for Preliminary Screening for Root-associating, Free-living Nitrogen-fixing Bacteria Inhabiting the Rhizoplane of Plants , 2002, Bioscience, biotechnology, and biochemistry.

[88]  R. Giegerich,et al.  GenDB--an open source genome annotation system for prokaryote genomes. , 2003, Nucleic acids research.

[89]  I. de Bruijn,et al.  Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. , 2006, Molecular plant-microbe interactions : MPMI.

[90]  J Davies,et al.  Novel natural products from soil DNA libraries in a streptomycete host. , 2000, Organic letters.

[91]  M. Bailey,et al.  Risk assessment for engineered bacteria used in biocontrol of fungal disease in agricultural crops , 2005, Plant and Soil.

[92]  Frank Oliver Glöckner,et al.  TETRA: a web-service and a stand-alone program for the analysis and comparison of tetranucleotide usage patterns in DNA sequences , 2004, BMC Bioinformatics.

[93]  L. Bakken,et al.  Evaluation of methods for extraction of bacteria from soil , 1995 .

[94]  J. Banfield,et al.  Genome-Directed Isolation of the Key Nitrogen Fixer Leptospirillum ferrodiazotrophum sp. nov. from an Acidophilic Microbial Community , 2005, Applied and Environmental Microbiology.

[95]  M. Breitbart,et al.  Using pyrosequencing to shed light on deep mine microbial ecology , 2006, BMC Genomics.

[96]  M. Pop,et al.  Metagenomic Analysis of the Human Distal Gut Microbiome , 2006, Science.

[97]  E. Koonin,et al.  Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. , 2000, Science.

[98]  R. Daniel,et al.  Enhancement of gene detection frequencies by combining DNA-based stable-isotope probing with the construction of metagenomic DNA libraries , 2006 .

[99]  Jo Handelsman,et al.  A Census of rRNA Genes and Linked Genomic Sequences within a Soil Metagenomic Library , 2003, Applied and Environmental Microbiology.

[100]  P. Oudemans,et al.  Characterization of a Chitinase Gene from Stenotrophomonas maltophilia Strain 34S1 and Its Involvement in Biological Control , 2002, Applied and Environmental Microbiology.

[101]  G. Jhon,et al.  Triacylglycerol, 1-Palmitoyl-2-Linoleoyl-3-Acetyl-rac -Glycerol Isolated from Bovine Udder and its Synthetic Enantiomer can Potentiate the Mitogenic Activity for Mouse Peritoneal Macrophages , 2003, Cellular Physiology and Biochemistry.

[102]  E. Delong,et al.  Microbial population genomics and ecology: the road ahead. , 2004, Environmental microbiology.

[103]  Donald L. Smith,et al.  Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes , 2005 .

[104]  Jizhong Zhou,et al.  Simultaneous Recovery of RNA and DNA from Soils and Sediments , 2001, Applied and Environmental Microbiology.

[105]  J. Clardy,et al.  Long-Chain N-Acyl Amino Acid Antibiotics Isolated from Heterologously Expressed Environmental DNA , 2000 .

[106]  K. Lewis,et al.  Isolating "Uncultivable" Microorganisms in Pure Culture in a Simulated Natural Environment , 2002, Science.

[107]  E. Madsen,et al.  Evaluation and Optimization of DNA Extraction and Purification Procedures for Soil and Sediment Samples , 1999, Applied and Environmental Microbiology.

[108]  J. Handelsman,et al.  Section 3 update: Isolation of high molecular weight genomic DNA from soil bacteria for genomic library construction , 2004 .

[109]  N. Ward New directions and interactions in metagenomics research. , 2006, FEMS microbiology ecology.

[110]  J. González-López,et al.  Isolation and characterization of Azotobacter and Azospirillum strains from the sugarcane rhizosphere , 2005, Plant and Soil.

[111]  T. Takagi,et al.  MetaGene: prokaryotic gene finding from environmental genome shotgun sequences , 2006, Nucleic acids research.

[112]  J. Handelsman Metagenomics: Application of Genomics to Uncultured Microorganisms , 2004, Microbiology and Molecular Biology Reviews.

[113]  S. Tringe,et al.  Comparative Metagenomics of Microbial Communities , 2004, Science.

[114]  K. Davies,et al.  Immunological quantification of the nematode parasitic bacterium Pasteuria penetrans in soil , 2001 .

[115]  Kim Rutherford,et al.  Artemis: sequence visualization and annotation , 2000, Bioinform..

[116]  Jianping Xu,et al.  INVITED REVIEW: Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances , 2006, Molecular ecology.

[117]  Jo Handelsman,et al.  Metagenomics for studying unculturable microorganisms: cutting the Gordian knot , 2005, Genome Biology.

[118]  R. M. Ray,et al.  Direct isolation of functional genes encoding cellulases from the microbial consortia in a thermophilic, anaerobic digester maintained on lignocellulose , 1995, Applied Microbiology and Biotechnology.

[119]  M. Arshad,et al.  Effect of plant growth promoting rhizobacteria containing ACC‐deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.) , 2006, Letters in applied microbiology.

[120]  Kun Zhang,et al.  Finding the Needles in the Metagenome Haystack , 2007, Microbial Ecology.

[121]  Jillian F. Banfield,et al.  Community genomics in microbial ecology and evolution , 2005, Nature Reviews Microbiology.

[122]  R. Amann Who is out there? Microbial aspects of biodiversity. , 2000, Systematic and applied microbiology.

[123]  Bryan A White,et al.  Suppressive subtractive hybridization as a tool for identifying genetic diversity in an environmental metagenome: the rumen as a model. , 2004, Environmental microbiology.

[124]  L. Handley,et al.  Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. , 2002, Molecular plant-microbe interactions : MPMI.

[125]  K. Watanabe,et al.  Detection of New Ethylene-Producing Bacteria, Pseudomonas syringae pvs. cannabina and sesami, by PCR Amplification of Genes for the Ethylene-Forming Enzyme. , 1997, Phytopathology.

[126]  J. Banfield,et al.  Community Proteomics of a Natural Microbial Biofilm , 2005, Science.

[127]  R. Müller,et al.  Recent developments towards the heterologous expression of complex bacterial natural product biosynthetic pathways. , 2005, Current opinion in biotechnology.

[128]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[129]  Genome Snapshot of Paenibacillus polymyxa ATCC 842 , 2006 .

[130]  J. Marchesi,et al.  Comparing the Dehalogenase Gene Pool in Cultivated α-Halocarboxylic Acid-Degrading Bacteria with the Environmental Metagene Pool , 2003, Applied and Environmental Microbiology.

[131]  A. Franks,et al.  Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[132]  Edward M. Rubin,et al.  Metagenomics: DNA sequencing of environmental samples , 2005, Nature Reviews Genetics.

[133]  B. Lugtenberg,et al.  Molecular basis of plant growth promotion and biocontrol by rhizobacteria. , 2001, Current opinion in plant biology.

[134]  S. Rigali,et al.  Pip, a Novel Activator of Phenazine Biosynthesis in Pseudomonas chlororaphisPCL1391 , 2006, Journal of bacteriology.

[135]  Jillian F Banfield,et al.  Population genomics in natural microbial communities. , 2006, Trends in ecology & evolution.

[136]  G. Lazarovits,et al.  Involvement of Quinolinate Phosphoribosyl Transferase in Promotion of Potato Growth by a Burkholderia Strain , 2006, Applied and Environmental Microbiology.

[137]  Anne K. Camper,et al.  Selective Removal of DNA from Dead Cells of Mixed Bacterial Communities by Use of Ethidium Monoazide , 2006, Applied and Environmental Microbiology.

[138]  R. J. Martinez,et al.  Identification of Members of the Metabolically Active Microbial Populations Associated with Beggiatoa Species Mat Communities from Gulf of Mexico Cold-Seep Sediments , 2004, Applied and Environmental Microbiology.

[139]  R. Daniel The metagenomics of soil , 2005, Nature Reviews Microbiology.

[140]  J. Wingender,et al.  Metagenome Survey of Biofilms in Drinking-Water Networks , 2003, Applied and Environmental Microbiology.

[141]  S. Salzberg,et al.  Improved microbial gene identification with GLIMMER. , 1999, Nucleic acids research.

[142]  Eoin L. Brodie,et al.  Environmental Whole-Genome Amplification To Access Microbial Populations in Contaminated Sediments , 2006, Applied and Environmental Microbiology.

[143]  M. Keller,et al.  Capturing the uncultivated majority. , 2006, Current opinion in biotechnology.

[144]  J. V. van Elsas,et al.  Application of polymerase chain reaction-denaturing gradient gel electrophoresis for comparison of direct and indirect extraction methods of soil DNA used for microbial community fingerprinting , 2000, Biology and Fertility of Soils.

[145]  C. Jacobsen Microscale detection of specific bacterial DNA in soil with a magnetic capture-hybridization and PCR amplification assay , 1995, Applied and environmental microbiology.

[146]  G. Holguin,et al.  Transformation of Azospirillum brasilense Cd with an ACC Deaminase Gene from Enterobacter cloacae UW4 Fused to the Tetr Gene Promoter Improves Its Fitness and Plant Growth Promoting Ability , 2003, Microbial Ecology.

[147]  G. M. Luna,et al.  DNA extraction procedure: a critical issue for bacterial diversity assessment in marine sediments. , 2006, Environmental microbiology.

[148]  S. Lindow,et al.  Utilization of the Plant Hormone Indole-3-Acetic Acid for Growth by Pseudomonas putida Strain 1290 , 2005, Applied and Environmental Microbiology.

[149]  K. Zengler,et al.  Cultivating the uncultured , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[150]  B. Glick,et al.  A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria , 1998, Journal of theoretical biology.

[151]  Jed Fuhrman,et al.  Whither or wither geomicrobiology in the era of 'community metagenomics' , 2005, Nature Reviews Microbiology.

[152]  C. Schmeisser,et al.  Metagenomics, biotechnology with non-culturable microbes , 2007, Applied Microbiology and Biotechnology.