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

  • Johan H. J. Leveau


This article aims to be a pragmatic primer into the field ofmetagenomics 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 ofthis review), a brief discussion about the technical problems and unrealistic expectations that are sometimes associated with metagenomics (the ’menace’), and a shortlist ofthe lessons that can be learned by those that wish to explore the utility ofmetagenomics in the study ofPGPR.


Metagenomics PGPR Plant growth-promoting rhizobacteria Environmental shotgun sequencing 


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  1. Abe, T., Sugawara, H., Kinouchi, M., Kanaya, S., & Ikemura, T. (2005). Novel phylogenetic studies of genomic sequence fragments derived from uncultured microbe mixtures in environmental and clinical samples. DNA Research, 12, 281–290.PubMedGoogle Scholar
  2. Abulencia, C. B., Wyborski, D. L., Garcia, J. A., Podar, M., Chen, W. Q., & Chang, S. H., et al. (2006). Environmental whole-genome amplification to access microbial populations in contaminated sediments. Applied and Environmental Microbiology, 72, 3291–3301.PubMedGoogle Scholar
  3. Allen, E. E., & Banfield, J. F. (2005). Community genomics in microbial ecology and evolution. Nature Reviews Microbiology, 3, 489–498.PubMedGoogle Scholar
  4. Amann, R. (2000). Who is out there? Microbial aspects of biodiversity. Systematic and Applied Microbiology, 23, 1–8.PubMedGoogle Scholar
  5. Basha, S., & Ulaganathan, K. (2002). Antagonism of Bacillus species (strain BC121) towards Curvularia lunata. Current Science, 82, 1457–1463.Google Scholar
  6. Béjà, O., Aravind, L., Koonin, E. V., Suzuki, M. T., Hadd, A., & Nguyen, L. P., et al. (2000a). Bacterial rhodopsin: Evidence for a new type of phototrophy in the sea. Science, 289, 1902–1906.PubMedGoogle Scholar
  7. Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M., & DeLong, E. F. (2001). Proteorhodopsin phototrophy in the ocean. Nature, 411, 786–789.PubMedGoogle Scholar
  8. Béjà, O., Suzuki, M. T., Koonin, E. V., Aravind, L., Hadd, A., & Nguyen, L. P., et al. (2000b). Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environmental Microbiology, 2, 516–529.PubMedGoogle Scholar
  9. Berry, A. E., Chiocchini, C., Selby, T., Sosio, M., & Wellington, E. M. H. (2003). Isolation of high molecular weight DNA from soil for cloning into BAC vectors. FEMS Microbiology Letters, 223, 15–20.PubMedGoogle Scholar
  10. Blaha, D., Sanguin, H., Robe, P., Nalin, R., Bally, R., & Moenne-Loccoz, Y. (2005). Physical organization of phytobeneficial genes nifH and ipdC in the plant growthpromoting rhizobacterium Azospirillum lipoferum 4V(I). FEMS Microbiology Letters, 244, 157–163.PubMedGoogle Scholar
  11. Bloemberg, G. V., & Lugtenberg, B. J. J. (2001). Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Current Opinion in Plant Biology, 4, 343–350.PubMedGoogle Scholar
  12. Brady, S. F., & Clardy, J. (2000). Long-chain n-acyl amino acid antibiotics isolated from heterologously expressed environmental DNA. Journal of the American Chemical Society, 122, 12903–12904.Google Scholar
  13. Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J. M., Segall, A. M., & Mead, D., et al. (2002). Genomic analysis of uncultured marine viral communities. Proceedings of the National Academy of Sciences USA, 99, 14250–14255.Google Scholar
  14. Bric, J. M., Bostock, R. M., & Silverstone, S. E. (1991). Rapid in situ assay for indoleacetic-acid production by bacteria immobilized on a nitrocellulose membrane. Applied and Environmental Microbiology, 57, 535–538.PubMedGoogle Scholar
  15. Buckley, D. H., & Schmidt, T. M. (2003). Diversity and dynamics of microbial communities in soils from agroecosystems. Environmental Microbiology, 5, 441–452.PubMedGoogle Scholar
  16. Chen, K., & Pachter, L. (2005). Bioinformatics for wholegenome shotgun sequencing of microbial communities. PLoS Computational Biology, 1, 106–112.PubMedGoogle Scholar
  17. Chin-A-Woeng, T. F. C., Bloemberg, G. V., van der Bij, A. J., van der Drift, K. M. G. F., Schripsema, J., & Kroon, B., et al. (1998). Biocontrol by phenazine-l-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicislycopersici. Molecular Plant-Microbe Interactions, 11, 1069–1077.Google Scholar
  18. Coeffet-Le Gal, M. F., Thurston, L., Rich, P., Miao, V., & Baltz, R. H. (2006). Complementation of daptomycin dptA and dptD deletion mutations in trans and production of hybrid lipopeptide antibiotics. Microbiology, 152, 2993–3001.PubMedGoogle Scholar
  19. Costa, R., Gotz, M., Mrotzek, N., Lottmann, J., Berg, G., & Smalla, K. (2006a). Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiology Ecology, 56, 236–249.PubMedGoogle Scholar
  20. Costa, R., Salles, J. F., Berg, G., & Smalla, K. (2006b). Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environmental Microbiology, 8, 2136–2149.PubMedGoogle Scholar
  21. Courtois, S., Cappellano, C. M., Ball, M., Francou, F. X., Normand, P., & Helynck, G., et al. (2003). Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Applied and Environmental Microbiology, 69, 49–55.PubMedGoogle Scholar
  22. Daniel, R. (2005). The metagenomics of soil. Nature Reviews Microbiology, 3, 470–478.PubMedGoogle Scholar
  23. Delcher, A. L., Harmon, D., Kasif, S., White, O., & Salzberg, S. L. (1999). Improved microbial gene identification with GLIMMER. Nucleic Acids Research, 27, 4636–4641.PubMedGoogle Scholar
  24. DeLong, E. F. (2004). Microbial population genomics and ecology: The road ahead. Environmental Microbiology, 6, 875–878.PubMedGoogle Scholar
  25. DeLong, E. F., Preston, C. M., Mincer, T., Rich, V., Hallam, S. J., & Frigaard, N. U., et al. (2006). Community genomics among stratified microbial assemblages in the ocean’s interior. Science, 311, 496–503.PubMedGoogle Scholar
  26. Deutschbauer, A. M., Chivian, D., & Arkin, A. P. (2006). Genomics for environmental microbiology. Current Opinion in Biotechnology, 17, 229–235.PubMedGoogle Scholar
  27. Devescovi, G., Aguilar, C., Majolini, M. B., Marugg, J., Weisbeek, P., & Venturi, V. (200 I). A siderophore peptide synthetase gene from plant growth-promoting Pseudomonas putida WCS358. Systematic and Applied Microbiology, 24, 321–330.Google Scholar
  28. Ding, Y., Wang, J., Liu, Y., & Chen, S. (2005). Isolation and identification of nitrogen-fixing bacilli from plant rhizospheres in Beijing region. Journal of Applied Microbiology, 99, 1271–1281.PubMedGoogle Scholar
  29. Downing, K., & Thomson, J. A. (2000). Introduction of the Serratia marcescens chiA gene into an endophytic Pseudomonas fluorescens for the biocontrol of phytopathogenic fungi. Canadian Journal ofMicrobiology, 46, 363–369.Google Scholar
  30. Dumont, M. G., Radajewski, S. M., Miguez, C. B., McDonald, I. R., & Murrell, J. C. (2006). Identification of a complete methane monooxygenase operon from soil by combining stable isotope probing and metagenomic analysis. Environmental Microbiology, 8, 1240–1250.PubMedGoogle Scholar
  31. Edwards, R. A., Rodriguez-Brito, B., Wegley, L., Haynes, M., Breitbart, M., & Peterson, D. M., et al. (2006). Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics, 7, 57.PubMedGoogle Scholar
  32. Edwards, R. A., & Rohwer, F. (2005). Viral metagenomics. Nature Reviews Microbiology, 3, 504–510.PubMedGoogle Scholar
  33. Emmert, E. A. B., Klimowicz, A. K., Thomas, M. G., & Handelsman, J. (2004). Genetics of Zwittermicin A production by Bacillus cereus. Applied and Environmental Microbiology, 70, 104–113.PubMedGoogle Scholar
  34. Entcheva, P., Liebl, W., Johann, A., Hartsch, T., & Streit, W. R. (2001). Direct cloning from enrichment cultures, a reliable strategy for isolation of complete operons and genes from microbial consortia. Applied and Environmental Microbiology, 67, 89–99.PubMedGoogle Scholar
  35. Erkel, C., Kube, M., Reinhardt, R., & Liesack, W. (2006). Genome of Rice Cluster I archaea — the key methane producers in the rice rhizosphere. Science, 313, 370–372.PubMedGoogle Scholar
  36. Fould, S., Dieng, A. L., Davies, K. G., Normand, P., & Mateille, T. (2001). Immunological quantification of the nematode parasitic bacterium Pasteuria penetrans in soil. FEMS Microbiology Ecology, 37, 187–195.Google Scholar
  37. Friedrich, M. W. (2006). Stable-isotope probing of DNA: Insights into the function of uncultivated microorganisms from isotopically labeled metagenomes. Current Opinion in Biotechnology, 17, 59–66.PubMedGoogle Scholar
  38. Fuhrman, J. A., Comeau, D. E., Hagstrom, A., & Chan, A. M. (1988). Extraction from natural planktonic microorganisms of DNA suitable for molecular biological studies. Applied and Environmental Microbiology, 54, 1426–1429.PubMedGoogle Scholar
  39. Gabor, E. M., Alkema, W. B. L., & Janssen, D. B. (2004a). Quantifying the accessibility of the metagenome by random expression cloning techniques. Environmental Microbiology, 6, 879–886.PubMedGoogle Scholar
  40. Gabor, E. M., de Vries, E. J., & Janssen, D. B. (2004b). Construction, characterization, and use of small-insert gene banks of DNA isolated from soil and enrichment cultures for the recovery of novel amidases. Environmental Microbiology, 6, 948–958.PubMedGoogle Scholar
  41. Galbraith, E. A., Antonopoulos, D. A., & White, B. A. (2004). Suppressive subtractive hybridization as a tool for identifying genetic diversity in an environmental metagenome: The rumen as a model. Environmental Microbiology, 6, 928–937.PubMedGoogle Scholar
  42. Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., & Samuel, B. S., et al. (2006). Metagenomic analysis of the human distal gut microbiome. Science, 312, 1355–1359.PubMedGoogle Scholar
  43. Girard, G., Barends, S., Rigali, S., van Rij, E. T., Lugtenberg, B. J. J., & Bloemberg, G. V. (2006). Pip, a novel activator of phenazine biosynthesis in Pseudomonas chlororaphis PCLI391. Journal ofBacteriology, 188, 8283–8293.Google Scholar
  44. Glick, B. R., & Bashan, Y. (1997). Genetic manipulation of plant growth-promoting bacteria to enhance biocontrol of phytopathogens. Biotechnology Advances, 15, 353–378.PubMedGoogle Scholar
  45. Glick, B. R., Penrose, D. M., & Li, J. P. (1998). A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. Journal of Theoretical Biology, 190, 63–68.PubMedGoogle Scholar
  46. Gohel, V., Megha, C., Vyas, P., & Chhatpar, H. S. (2004). Strain improvement of chitinolytic enzyme producing isolate Pantoea dispersa for enhancing its biocontrol potential against fungal plant pathogens. Annals of Microbiology, 54, 503–515.Google Scholar
  47. Grant, S., Grant, W. D., Cowan, D. A., Jones, B. E., Ma, Y. H., & Ventosa, A., et al. (2006). Identification of eukaryotic open reading frames in metagenomic cDNA libraries made from environmental samples. Applied and Environmental Microbiology, 72, 135–143.PubMedGoogle Scholar
  48. Gray, E. J., & Smith, D. L. (2005). Intracellular and extracellular PGPR: Commonalities and distinctions in the plant-bacterium signaling processes. Soil Biology & Biochemistry, 37, 395–412.Google Scholar
  49. Green, B. D., & Keller, M. (2006). Capturing the uncultivated majority. Current Opinion in Biotechnology, 17, 236–240.PubMedGoogle Scholar
  50. Gremion, F., Chatzinotas, A., & Harms, H. (2003). 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. Environmental Microbiology, 5, 896–907.PubMedGoogle Scholar
  51. Hallam, S. J., Putnam, N., Preston, C. M., Detter, J. C., Rokhsar, D., & Richardson, P. M., et al. (2004). Reverse methanogenesis: Testing the hypothesis with environmental genomics. Science, 305, 1457–1462.PubMedGoogle Scholar
  52. Handelsman, J. (2004). Metagenomics: Application of genomics to uncultured microorganisms. Microbiology and Molecular Biology Reviews, 68, 669–685.PubMedGoogle Scholar
  53. Handelsman, J. (2005). Metagenomics or megagenomics? Nature Reviews Microbiology, 3, 457–458.Google Scholar
  54. Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J., & Goodman, R. M. (1998). Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products. Chemistry & Biology, 5, R245–R249.Google Scholar
  55. Hashidoko, Y., Tada, M., Osaki, M., & Tahara, S. (2002). Soft gel medium solidified with gellan gum for preliminary screening for root-associating, free-living nitrogen-fixing bacteria inhabiting the rhizoplane of plants. Bioscience Biotechnology and Biochemistry, 66, 2259–2263.Google Scholar
  56. Healy, F. G., Ray, R. M., Aldrich, H. C., Wilkie, A. C., Ingram, L. O., & Shanmugam, K. T. (1995). Direct isolation of functional genes encoding cellulases from the microbial consortia in a thermophilic, anaerobic digester maintained on lignocellulose. Applied Microbiology and Biotechnology, 43, 667–674.PubMedGoogle Scholar
  57. Henne, A., Daniel, R., Schmitz, R. A., & Gottschalk, G. (1999). Construction of environmental DNA libraries in Escherichia coli and screening for the presence of genes conferring utilization of 4-hydroxybutyrate. Applied and Environmental Microbiology, 65, 3901–3907.PubMedGoogle Scholar
  58. Holguin, G., & Glick, B. R. (2003). Transformation of Azospirillum brasilense Cd with an ACC deaminase gene from Enterobacter cloacae UW4 fused to the Tet(r) gene promoter improves its fitness and plant growth promoting ability. Microbial Ecology, 46, 122–133.PubMedGoogle Scholar
  59. Hurek, T., Handley, L. L., Reinhold-Hurek, B., & Piche, Y. (2002). Azoarcus. grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Molecular Plant-Microbe Interactions, 15, 233–242.PubMedGoogle Scholar
  60. Hurt, R. A., Qiu, X. Y., Wu, L. Y., Roh, Y., Palumbo, A. V., & Tiedje, J. M., et al. (2001). Simultaneous recovery ofRNA and DNA from soils and sediments. Applied and Environmental Microbiology, 67, 4495–4503.PubMedGoogle Scholar
  61. Jacobsen, C. S. (1995). Microscale detection of specific bacterial-DNA in soil with a magnetic capture-hybridization and PCR amplification assay. Applied and Environmental Microbiology, 61, 3347–3352.PubMedGoogle Scholar
  62. Jacobsen, C. S. (2004). Purification of microbial genes from soil and rhizosphere by magnetic capture hybridization and subsequent amplification of target genes by PCR. In: G. A. Kowalchuk, F.J. De Bruijn, I. M. Head, A. D. L. Akkermans, J. D. Van Elsas (Eds.), Molecular microbialecology manual (pp. 181–188). Dordrecht, The Netherlands: Kluwer.Google Scholar
  63. Jeong, H., Kim, J. F., Park, Y. K., Kim, S. B., Kim, C., & Park, S. H. (2006). Genome snapshot of Paenibacilluspolymyxa ATCC 842. Journal of Microbiology and Biotechnology, 16, 1650–1655.Google Scholar
  64. Jiao, J. Y., Wang, H. X., Zeng, Y., & Shen, Y. M. (2006). Enrichment for microbes living in association with plant tissues. Journal ofApplied Microbiology, 100, 830–837.Google Scholar
  65. Joseph, S. J., Hugenholtz, P., Sangwan, P., Osburne, C. A., & Janssen, P. H. (2003). Laboratory cultivation of widespread and previously uncultured soil bacteria. Applied and Environmental Microbiology, 69, 7210–7215.PubMedGoogle Scholar
  66. Juraeva, D., George, E., Davranov, K., & Ruppel, S. (2006). Detection and quantification of the nifH gene in shoot and root of cucumber plants. Canadian Journal of Microbiology, 52, 731–739.PubMedGoogle Scholar
  67. Kaeberlein, T., Lewis, K., & Epstein, S. S. (2002). Isolating ‘uncultivable’ microorganisms in pure culture by a simulated natural environment. Science, 296, 1127–1129.PubMedGoogle Scholar
  68. Kim, J., Kim, E., Kang, Y., Choi, O., Park, C. S., & Hwang, I. (2006). Molecular characterization of biosynthetic genes of an antifungal compound produced by Pseudomonas fluorescens MC07. Journal of Microbiology and Biotechnology, 16, 450–456.Google Scholar
  69. Kloepper, J. W., & Schroth, M. N. (1978). Plant growth-promoting rhizobacteria in radish. In: Proceedings of the 4th International Conference on Plant Pathogenic Bacteria (pp. 879–882), INRA, Angers, France.Google Scholar
  70. Knietsch, A., Bowien, S., Whited, G., Gottschalk, G., & Daniel, R. (2003a). Identification and characterization of coenzyme B-12-dependent glycerol dehydratase-and diol dehydratase-encoding genes from metagenomic DNA libraries derived from enrichment cultures. Applied and EnvironmentalMicrobiology, 69, 3048–3060.Google Scholar
  71. Knietsch, A., Waschkowitz, T., Bowien, S., Henne, A., & Daniel, R. (2003b). Construction and screening of metagenomic libraries derived from enrichment cultures: Generation of a gene bank for genes conferring alcohol oxidoreductase activity on Escherichia coli. Applied and Environmental Microbiology, 69, 1408–1416.PubMedGoogle Scholar
  72. Kobayashi, D. Y., Reedy, R. M., Bick, J., & Oudemans, P. V. (2002). Characterization of a chitinase gene from Stenotrophomonas maltophilia strain 34S1 and its involvement in biological control. Applied and Environmental Microbiology, 68, 1047–1054.PubMedGoogle Scholar
  73. Kowalchuk, G. A., de Bruijn, F. J., Head, I. M., Akkermans, A. D. L., & van Elsas, J. D. (2004). Molecular microbial ecology manual.Dordrecht, The Netherlands: Kluwer.Google Scholar
  74. Kowalchuk, G. A., Speksnijder, A. G. C. L., Zhang, K., Goodman, R. M., & van Veen, J. A. (2007). Finding the needles in the metagenome haystack. Microbial Ecology, 53, 475–485.PubMedGoogle Scholar
  75. Kozdroj, J., & van Elsas, J. D. (2000). 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. Biology and Fertility of Soils, 31, 372–378.Google Scholar
  76. Lee, E. T., Lim, S. K., Nam, D. H., Khang, Y. H., & Kim, S. D. (2003). Pyoverdin(2112) of Pseudomonas fluorescens 2112 inhibits Phytophthora capsici, a red-pepper blight-causing fungus. Journal ofMicrobiology and Biotechnology, 13, 415–421.Google Scholar
  77. Leveau, J. H. J., Gerards, S., de Boer, W., & van Veen, J. A. (2004). Phylogeny-function analysis of (meta)genomic libraries: Screening for expression of ribosomal RNA genes by large-insert library fluorescent in situ hybridization (LILFISH). Environmental Microbiology, 6, 990–998.PubMedGoogle Scholar
  78. Leveau, J. H. J., Gerards, S., Fritsche, K., Zondag, G., & van Veen, J. A. (2006). Genomic flank-sequencing of plasposon insertion sites for rapid identification of functional genes. Journal ofMicrobiological Methods, 66, 276–285.Google Scholar
  79. Leveau, J. H. J., & Lindow, S. E. (2005). Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Applied and Environmental Microbiology, 71, 2365–2371.PubMedGoogle Scholar
  80. Li, Y. G., Wexler, M., Richardson, D. J., Bond, P. L., & Johnston, A. W. B. (2005). 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. Environmental Microbiology, 7, 1927–1936.PubMedGoogle Scholar
  81. Liles, M. R., Manske, B. F., Bintrim, S. B., Handelsman, J., & Goodman, R. M. (2003). A census ofrRNA genes and linked genomic sequences within a soil metagenomic library. Applied and Environmental Microbiology, 69, 2684–2691.PubMedGoogle Scholar
  82. Liles, M. R., Williamson, L. L., Handelsman, J., & Goodman, R. M. (2004). Isolation of high molecular weight genomic DNA from soil bacteria for genomic library construction. In G. A. Kowalchuk, F. J. De Bruijn, I. M. Head, A. D. L. Akkermans, & J. D. Van Elsas (Eds.) Molecular microbial ecology manual (pp. 839–849)). Dordrecht, The Netherlands: Kluwer.Google Scholar
  83. Lindahl, V., & Bakken, L. R. (1995). Evaluation of methods for extraction of bacteria from soil. FEMS Microbiology Ecology, 16, 135–142.Google Scholar
  84. Lorenz, P., & Eck, J. (2005). Metagenomics and industrial applications. Nature Reviews Microbiology, 3, 510–516.PubMedGoogle Scholar
  85. Lucy, M., Reed, E., & Glick, B. R. (2004). Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek, 86, 1–25.PubMedGoogle Scholar
  86. Luna, G. M., Dell’Anno, A., & Danovaro, R. (2006). DNA extraction procedure: A critical issue for bacterial diversity assessment in marine sediments. Environmental Microbiology, 8, 308–320.PubMedGoogle Scholar
  87. Majernik, A., Gottschalk, G., & Daniel, R. (2001). 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. Journal of Bacteriology, 183, 6645–6653.PubMedGoogle Scholar
  88. Marchesi, J. R., & Weightman, A. J. (2003). Comparing the dehalogenase gene pool in cultivated. a.-halocarboxylic aciddegrading bacteria with the environmental metagene pool. Applied and Environmental Microbiology, 69, 4375–4382.PubMedGoogle Scholar
  89. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., & Bemben, L. A., et al. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.PubMedGoogle Scholar
  90. Mark, G. L., Dow, J. M., Kiely, P. D., Higgins, H., Haynes, J., & Baysse, C., et al. (2005). Transcriptome profiling ofbacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proceedings of the National Academy ofSciences USA, 102, 17454–17459.Google Scholar
  91. Martinez, A., Kolvek, S. J., Yip, C. L. T., Hopke, J., Brown, K. A., & MacNeil, J. A., et al. (2004). Genetically modified bacterial strains and novel bacterial artificial chromosome shuttle vectors for constructing environmental libraries and detecting heterologous natural products in multiple expression hosts. Applied and Environmental Microbiology, 70, 2452–2463.PubMedGoogle Scholar
  92. Meyer, F., Goesmann, A., McHardy, A. C., Bartels, D., Bekel, T., & Clausen, J., et al. (2003). GenDB — An open source genome annotation system for prokaryote genomes. Nucleic Acids Research, 31, 2187–2195.PubMedGoogle Scholar
  93. Miller, D. N., Bryant, J. E., Madsen, E. L., & Ghiorse, W. C. (1999). Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Applied and Environmental Microbiology, 65, 4715–4724.PubMedGoogle Scholar
  94. Millner, P. D., & Wright, S. E (2002). Tools for support of ecological research on arbuscular mycorrhizal fungi. Symbiosis, 33, 101–123.Google Scholar
  95. Mills, H. J., Martinez, R. J., Story, S., & Sobecky, P. A. (2004). Identification of members of the metabolically active microbial populations associated with Beggiatoa species mat communities form Gulf of Mexico cold-seep sediments. Applied and Environmental Microbiology, 70, 5447–5458.PubMedGoogle Scholar
  96. Nesbe, C. L., Boucher, Y., Dlutek, M., & Doolittle, W. F. (2005). Lateral gene transfer and phylogenetic assignment of environmental fosmid clones. Environmental Microbiology, 7, 2011–2026.Google Scholar
  97. Nocker, A., & Camper, A. K. (2006). Selective removal of DNA from dead cells of mixed bacterial communities by use of ethidium monoazide. Applied and Environmental Microbiology, 72, 1997–2004.PubMedGoogle Scholar
  98. Noguchi, H., Park, J., & Takagi, T. (2006). MetaGene: Prokaryotic gene fmding from environmental genome shotgun sequences. Nucleic Acids Research, 34, 5623–5630.PubMedGoogle Scholar
  99. Orner, Z. S., Tombolini, R., Broberg, A., & Gerhardson, B. (2004). Indole-3-acetic acid production by pink-pigmented facultative methylotrophic bacteria. Plant Growth Regulation, 43, 93–96.Google Scholar
  100. Oremland, R. S., Capone, D. G., Stolz, J. E, & Fuhrman, J. (2005). Whither or wither geomicrobiology in the era of “community metagenomics”. Nature Reviews Microbiology, 3, 572–578.PubMedGoogle Scholar
  101. Poretsky, R. S., Bano, N., Buchan, A., LeCleir, G., Kleikemper, J., & Pickering, M., et al. (2005). Analysis of microbial gene transcripts in environmental samples. Applied and Environmental Microbiology, 71, 4121–4126.PubMedGoogle Scholar
  102. Quaiser, A., Ochsenreiter, T., Klenk, H. P., Kletzin, A., Treusch, A. H., & Meurer, G., et al. (2002). First insight into the genome of an uncultivated crenarchaeote from soil. Environmental Microbiology, 4, 603–611.PubMedGoogle Scholar
  103. Quaiser, A., Ochsenreiter, T., Lanz, C., Schuster, S. C., Treusch, A. H., & Eck, J., et al. (2003). Acidobacteria form a coherent but highly diverse group within the bacterial domain: Evidence from environmental genomics. Molecular Microbiology, 50, 563–575.PubMedGoogle Scholar
  104. Raaijmakers, J. M., de Bruijn, J., & de Kock, M. J. D. (2006). Cyclic lipopeptide production by plant-associated Pseudomonas spp.: Diversity, activity, biosynthesis, and regulation. Molecular Plant-Microbe Interactions, 19, 699–710.PubMedGoogle Scholar
  105. Radwan, T., Mohamed, Z. K., & Reis, V. M. (2002). Production of indole-3-acetic acid by different strains of Azospirillum and Herbaspirillum spp. Symbiosis, 32, 39–53.Google Scholar
  106. Rajendran, N., Rompf, A., Marahiel, M. A., & Jahn, D. (1998). Isolation and characterization of a transposon mutant of Pseudomonas fluorescens AU63 deficient in antifungal activity against Pythium ultimum. Letters in Applied Microbiology, 27, 152–157.Google Scholar
  107. Ram, R. J., VerBerkmoes, N. C., Thelen, M. P., Tyson, G. W., Baker, B. J., & Blake, R. C., et al. (2005). Community proteomics ofa natural microbial biofilm. Science, 308, 1915–1920.PubMedGoogle Scholar
  108. Rangarajan, S., Saleena, L. M., Vasudevan, P., & Nair, S. (2003). Biological suppression ofrice diseases by Pseudomonas spp. under saline soil conditions. Plant and Soil, 251, 73–82.Google Scholar
  109. Riesenfeld, C. S., Goodman, R. M., & Handelsman, J. (2004a). Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environmental Microbiology, 6, 981–989.PubMedGoogle Scholar
  110. Riesenfeld, C. S., Schloss, P. D., & Handelsman, J. (2004b). Metagenomics: Genomic analysis of microbial communities. Annual Reviews in Genetics, 38, 525–552.Google Scholar
  111. Rodriguez, H., Gonzalez, T., & Selman, G. (2000). Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. Journal of Biotechnology, 84, 155–161.Google Scholar
  112. Rodriguez-Brito, B., Rohwer, F., & Edwards, R. A. (2006). An application of statistics to comparative metagenomics. BMC Bioinformatics, 7, 162.PubMedGoogle Scholar
  113. Rondon, M. R., August, P. R., Bettermann, A. D., Brady, S. F., Grossman, T. H., & Liles, M. R., et al. (2000). Cloning the soil metagenome: A strategy for accessing the genetic and functional diversity of uncultured microorganisms. Applied and Environmental Microbiology, 66, 2541–2547.PubMedGoogle Scholar
  114. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., & Rajandream, M. A. (2000). Artemis: Sequence visualization and annotation. Bioinform atics, 16, 944–945.Google Scholar
  115. Sanger, F., Nicklen, S., & Coulson, A. R. (1977). DNA Sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America, 74, 5463–5467.PubMedGoogle Scholar
  116. Sanguin, H., Remenant, B., Dechesne, A., Thioulouse, J., Vogel, T. M., & Nesme, X., et al. (2006). Potential of a 16S rRNA-based taxonomic microarray for analyzing the rhizosphere effects of maize on Agrobacterium spp. and bacterial communities. Applied and Environmental Microbiology, 72, 4302–4312.PubMedGoogle Scholar
  117. Sato, M., Watanabe, K., Yazawa, M., Takikawa, Y., & Nishiyama, K. (1997). Detection of new ethylene-producing bacteria, Pseudomonas syringae pvs. cannabina and sesami, by PCR amplification of genes for the ethyleneforming enzyme. Phytopathology, 87, 1192–1196.PubMedGoogle Scholar
  118. Schloss, P. D., & Handelsman, J. (2005). Metagenomics for studying unculturable microorganisms: Cutting the Gordian knot. Genome Biology, 6, 229.PubMedGoogle Scholar
  119. Schmeisser, C., Steele, H., & Streit, W. R. (2007). Metagenomics, biotechnology with non-cu1turable microbes. Applied Microbiology and Biotechnology, 75, 955–962.PubMedGoogle Scholar
  120. Schmeisser, C., Stockigt, C., Raasch, C., Wingender, J., Timmis, K. N., & Wenderoth, D. F., et al. (2003). Metagenome survey ofbiofilms in drinking-water networks. Applied and Environmental Microbiology, 69, 7298–7309.PubMedGoogle Scholar
  121. Schmidt, T. M., Delong, E. F., & Pace, N. R. (1991). Analysis of a marine picoplankton community by 16S ribosomalRNA gene cloning and sequencing. Journal of Bacteriology, 173, 4371–4378.PubMedGoogle Scholar
  122. Schwarz, S., Waschkowitz, T., & Daniel, R. (2006). Enhancement of gene detection frequencies by combining DNAbased stable-isotope probing with the construction of metagenomic DNA libraries. World Journal ofMicrobiology & Biotechnology, 22, 363–367.Google Scholar
  123. Shah, S., Li, J. P., Moffatt, B. A., & Glick, B. R. (1998). Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Canadian Journal of Microbiology, 44, 833–843.PubMedGoogle Scholar
  124. Shaharoona, B., Arshad, M., & Zahir, Z. A. (2006). Effect of plant growth-promoting rhizobacteria containing ACCdeaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Letters in Applied Microbiology, 42, 155–159.PubMedGoogle Scholar
  125. Sliwinski, M. K., & Goodman, R. M. (2004). Comparison of crenarchaeal consortia inhabiting the rhizosphere of diverse terrestrial plants with those in bulk soil in native environments. Applied and Environmental Microbiology, 70, 1821–1826.PubMedGoogle Scholar
  126. Sreenivasan, A. (2001). Earth’s anonymous inhabitants. In: Science Notes, an online magazine produced by the graduate students in the Science Communication Program at the University of California, Santa Cruz (URL to the article: Scholar
  127. Staunton, J., & Weissman, K. J.(2001). Polyketide biosynthesis: A millennium review. Natural Product Reports, 18, 380–416.PubMedGoogle Scholar
  128. Stevenson, B. S., Eichorst, S. A., Wertz, J. T., Schmidt, T. M., & Breznak, J. A. (2004). New strategies for cultivation and detection of previously uncultured microbes. Applied and Environmental Microbiology, 70, 4748–4755.PubMedGoogle Scholar
  129. Streit, W. R., & Schmitz, R. A. (2004). Metagenomics — The key to the uncultured microbes. Current Opinion in Microbiology, 7, 492–498.PubMedGoogle Scholar
  130. Tebbe, C. C., & Vahjen, W. (1993). Interference of humic acids and DNA extracted directly from soil in detection and transformation of recombinant-DNA from bacteria and a yeast. Applied and Environmental Microbiology, 59, 2657–2665.PubMedGoogle Scholar
  131. Teeling, H., Waldmann, J., Lombardot, T., Bauer, M., & Glockner, F. O. (2004). TETRA: A web-service and a stand-alone program for the analysis and comparison of tetranucleotide usage patterns in DNA sequences. BMC Bioinformatics, 5, 163.PubMedGoogle Scholar
  132. Tejera, N., Lluch, C., Martinez-Toledo, M. V., & GonzalezLopez, J. (2005). Isolation and characterization of Azotobacter and Azospirillum strains from the sugarcane rhizosphere. Plant and Soil, 270, 223–232.Google Scholar
  133. Timms-Wilson, T. M., Kilshaw, K., & Bailey, M. J. (2004). Risk assessment for engineered bacteria used in biocontrol of fungal disease in agricultural crops. Plant and Soil, 266, 57–67.Google Scholar
  134. Timmusk, S., Nicander, B., Granhall, U., & Tillberg, E. (1999). Cytokinin production by Paenibacillus polymyxa. Soil Biology & Biochemistry, 31, 1847–1852.Google Scholar
  135. Tringe, S. G., & Rubin, E. M. (2005). Metagenomics: DNA sequencing of environmental samples. Nature Reviews Genetics, 6, 805–814.PubMedGoogle Scholar
  136. Tringe, S. G., von Mering, C., Kobayashi, A., Salamov, A. A., Chen, K., & Chang, H. W., et al. (2005). Comparative metagenomics of microbial communities. Science, 308, 554–557.PubMedGoogle Scholar
  137. Tyson, G. W., Chapman, J., Hugenholtz, P., Allen, E. E., Ram, R. J., & Richardson, P. M., et al. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature, 428, 37–43.PubMedGoogle Scholar
  138. Tyson, G. W., Lo, I., Baker, B. J., Allen, E. E., Hugenholtz, P., & Banfield, J. F. (2005). Genome-directed isolation of the key nitrogen fixer Leptospirillum ferrodiazotrophum sp nov from an acidophilic microbial community. Applied and Environmental Microbiology, 71, 6319–6324.PubMedGoogle Scholar
  139. Uchiyama, T., Abe, T., Ikemura, T., & Watanabe, K. (2005). Substrate-induced gene-expression screening of environmental metagenome libraries for isolation of catabolic genes. Nature Biotechnology, 23, 88–93.PubMedGoogle Scholar
  140. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., & Sutton, G. G., et al. (2001). The sequence of the human genome. Science, 291, 1304–1351.PubMedGoogle Scholar
  141. Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., & Eisen, J. A., et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304, 66–74.PubMedGoogle Scholar
  142. Vessey, J. K. (2003). Plant growth-promoting rhizobacteria as biofertilizers. Plant and Soil, 255, 571–586.Google Scholar
  143. Wagner, M., & Hom, M. (2006). The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Current Opinion in Biotechnology, 17, 241–249.PubMedGoogle Scholar
  144. Wang, K., Conn, K., & Lazarovits, G. (2006). Involvement of quinolinate phosphoribosyl transferase in promotion of potato growth by a Burkholderia strain. Applied and Environmental Microbiology, 72,760–768.PubMedGoogle Scholar
  145. Wang, G. Y. S., Graziani, E., Waters, B., Pan, W., Li, X., & McDermott, J., et al. (2000). Novel natural products from soil DNA libraries in a Streptomycete host. Organic Letters, 2, 2401–2404.PubMedGoogle Scholar
  146. Wang, Y. Q., Ohara, Y., Nakayashiki, H., Tosa, Y.,& Mayama, S. (2005). Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Molecular Plant-Microbe Interactions, 18, 385–396.PubMedGoogle Scholar
  147. Ward, N. (2006). New directions and interactions in metagenomics research. FEMS Microbiology Ecology, 55, 331–338.PubMedGoogle Scholar
  148. Weller, D. M., Raaijmakers, J. M., Gardener, B. B. M., & Thomashow, L. S. (2002). Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 40, 309–348.PubMedGoogle Scholar
  149. Wenzel, S. C., & Müller, R. (2005). Recent developments towards the heterologous expression of complex bacterial natural product biosynthetic pathways. Current Opinion in Biotechnology, 16, 594–606.PubMedGoogle Scholar
  150. Whitaker, R. J., & Banfield, J. F. (2006). Population genomics in natural microbial communities. Trends in Ecology & Evolution, 21, 508–516.Google Scholar
  151. Williamson, L. L., Borlee, B. R., Schloss, P. D., Guan, C. H., Allen, H. K., & Handelsman, J. (2005). Intracellular screen to identify metagenomic clones that induce or inhibit a quorum-sensing biosensor. Applied and Environmental Microbiology, 71, 6335–6344.PubMedGoogle Scholar
  152. Woyke, T., Teeling, H., Ivanova, N. N., Huntemann, M., Richter, M., & Gloeckner, F. O., et al. (2006). Symbiosis insights through metagenomic analysis of a microbial consortium. Nature, 443, 950–955.PubMedGoogle Scholar
  153. Xu, J. P. (2006). Microbial ecology in the age of genomics and metagenomics: Concepts, tools, and recent advances. Molecular Ecology, 15, 1713–1731.PubMedGoogle Scholar
  154. Zengler, K., Toledo, G., Rappe, M., Elkins, J., Mathur, E. J., & Short, J. M., et al. (2002). Cultivating the uncultured. Proceedings of the National Academy of Sciences of the United States ofAmerica, 99, 15681–15686.Google Scholar
  155. Zhou, J. Z., Bruns, M. A., & Tiedje, J. M. (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62, 316–322.PubMedGoogle Scholar

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© KNPV 2007

Authors and Affiliations

  1. 1.Netherlands Institute of Ecology (NIOO-KNAW)HeterenThe Netherlands

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