Genomics & Informatics

Korea Genome Organization (한국유전체학회)
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Bioprospecting Potential of the Soil Metagenome: Novel Enzymes and Bioactivities

  • Received : 2013.07.09
  • Accepted : 2013.08.20
  • Published : 2013.09.30
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Abstract

The microbial diversity in soil ecosystems is higher than in any other microbial ecosystem. The majority of soil microorganisms has not been characterized, because the dominant members have not been readily culturable on standard cultivation media; therefore, the soil ecosystem is a great reservoir for the discovery of novel microbial enzymes and bioactivities. The soil metagenome, the collective microbial genome, could be cloned and sequenced directly from soils to search for novel microbial resources. This review summarizes the microbial diversity in soils and the efforts to search for microbial resources from the soil metagenome, with more emphasis on the potential of bioprospecting metagenomics and recent discoveries.

Keywords

References

  1. Staley JT, Konopka A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 1985;39:321-346. https://doi.org/10.1146/annurev.mi.39.100185.001541
  2. Pace NR, Stahl DA, Lane DJ, Olsen GJ. Analyzing natural microbial populations by rRNA sequences. ASM News 1985; 51:4-12.
  3. Torsvik V, $\phi$vreas L, Thingstad TF. Prokaryotic diversity: magnitude, dynamics, and controlling factors. Science 2002;296: 1064-1066. https://doi.org/10.1126/science.1071698
  4. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 1998;95:6578-6583. https://doi.org/10.1073/pnas.95.12.6578
  5. Torsvik V, Goksøyr J, Daae FL. High diversity in DNA of soil bacteria. Appl Environ Microbiol 1990;56:782-787.
  6. Torsvik V, Sørheim R, Goksøyr J. Total bacterial diversity in soil and sediment communities: a review. J Ind Microbiol 1996;17:170-178. https://doi.org/10.1007/BF01574690
  7. Amann RI, Ludwig W, Schleifer KH. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 1995;59:143-169.
  8. Delmont TO, Robe P, Cecillon S, Clark IM, Constancias F, Simonet P, et al. Accessing the soil metagenome for studies of microbial diversity. Appl Environ Microbiol 2011;77:1315- 1324. https://doi.org/10.1128/AEM.01526-10
  9. Janssen PH. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 2006;72:1719-1728. https://doi.org/10.1128/AEM.72.3.1719-1728.2006
  10. Lim HK, Chung EJ, Kim JC, Choi GJ, Jang KS, Chung YR, et al. Characterization of a forest soil metagenome clone that confers indirubin and indigo production on Escherichia coli. Appl Environ Microbiol 2005;71:7768-7777. https://doi.org/10.1128/AEM.71.12.7768-7777.2005
  11. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 2011;332:1097-1100. https://doi.org/10.1126/science.1203980
  12. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 1998;5:R245-R249. https://doi.org/10.1016/S1074-5521(98)90108-9
  13. Healy FG, Ray RM, Aldrich HC, Wilkie AC, Ingram LO, Shanmugam KT. Direct isolation of functional genes encoding cellulases from the microbial consortia in a thermophilic, anaerobic digester maintained on lignocellulose. Appl Microbiol Biotechnol 1995;43:667-674. https://doi.org/10.1007/BF00164771
  14. Berry AE, Chiocchini C, Selby T, Sosio M, Wellington EM. Isolation of high molecular weight DNA from soil for cloning into BAC vectors. FEMS Microbiol Lett 2003;223:15-20. https://doi.org/10.1016/S0378-1097(03)00248-9
  15. Ogram A, Sayler GS, Barkay T. The extraction and purification of microbial DNA from sediments. J Microbiol Methods 1987;7:57-66. https://doi.org/10.1016/0167-7012(87)90025-X
  16. Zhou J, Bruns MA, Tiedje JM. DNA recovery from soils of diverse composition. Appl Environ Microbiol 1996;62:316-322.
  17. Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, et al. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 2000;66: 2541-2547. https://doi.org/10.1128/AEM.66.6.2541-2547.2000
  18. Kim UJ, Shizuya H, de Jong PJ, Birren B, Simon MI. Stable propagation of cosmid sized human DNA inserts in an F factor based vector. Nucleic Acids Res 1992;20:1083-1085. https://doi.org/10.1093/nar/20.5.1083
  19. Chung EJ, Lim HK, Kim JC, Choi GJ, Park EJ, Lee MH, et al. Forest soil metagenome gene cluster involved in antifungal activity expression in Escherichia coli. Appl Environ Microbiol 2008;74:723-730. https://doi.org/10.1128/AEM.01911-07
  20. Bertrand H, Poly F, Van VT, Lombard N, Nalin R, Vogel TM, et al. High molecular weight DNA recovery from soils prerequisite for biotechnological metagenomic library construction. J Microbiol Methods 2005;62:1-11. https://doi.org/10.1016/j.mimet.2005.01.003
  21. Iqbal HA, Feng Z, Brady SF. Biocatalysts and small molecule products from metagenomic studies. Curr Opin Chem Biol 2012;16:109-116. https://doi.org/10.1016/j.cbpa.2012.02.015
  22. Simon C, Daniel R. Metagenomic analyses: past and future trends. Appl Environ Microbiol 2011;77:1153-1161. https://doi.org/10.1128/AEM.02345-10
  23. Lee SW, Won K, Lim HK, Kim JC, Choi GJ, Cho KY. Screening for novel lipolytic enzymes from uncultured soil microorganisms. Appl Microbiol Biotechnol 2004;65:720-726. https://doi.org/10.1007/s00253-004-1722-3
  24. Wang C, Meek DJ, Panchal P, Boruvka N, Archibald FS, Driscoll BT, et al. Isolation of poly-3-hydroxybutyrate metabolism genes from complex microbial communities by phenotypic complementation of bacterial mutants. Appl Environ Microbiol 2006;72:384-391. https://doi.org/10.1128/AEM.72.1.384-391.2006
  25. Uchiyama T, Abe T, Ikemura T, Watanabe K. Substrate-induced gene-expression screening of environmental metagenome libraries for isolation of catabolic genes. Nat Biotechnol 2005;23:88-93. https://doi.org/10.1038/nbt1048
  26. Williamson LL, Borlee BR, Schloss PD, Guan C, Allen HK, Handelsman J. Intracellular screen to identify metagenomic clones that induce or inhibit a quorum-sensing biosensor. Appl Environ Microbiol 2005;71:6335-6344. https://doi.org/10.1128/AEM.71.10.6335-6344.2005
  27. Uchiyama T, Miyazaki K. Product-induced gene expression, a product-responsive reporter assay used to screen metagenomic libraries for enzyme-encoding genes. Appl Environ Microbiol 2010;76:7029-7035. https://doi.org/10.1128/AEM.00464-10
  28. Craig JW, Chang FY, Kim JH, Obiajulu SC, Brady SF. Expanding small-molecule functional metagenomics through parallel screening of broad-host-range cosmid environmental DNA libraries in diverse proteobacteria. Appl Environ Microbiol 2010;76:1633-1641. https://doi.org/10.1128/AEM.02169-09
  29. Knietsch A, Bowien S, Whited G, Gottschalk G, Daniel R. Identification and characterization of coenzyme B12-dependent glycerol dehydratase- and diol dehydratase-encoding genes from metagenomic DNA libraries derived from enrichment cultures. Appl Environ Microbiol 2003;69:3048-3060. https://doi.org/10.1128/AEM.69.6.3048-3060.2003
  30. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, et al. Functional metagenomic profiling of nine biomes. Nature 2008;452:629-632. https://doi.org/10.1038/nature06810
  31. Teeling H, Glockner FO. Current opportunities and challenges in microbial metagenome analysis: a bioinformatic perspective. Brief Bioinform 2012;13:728-742. https://doi.org/10.1093/bib/bbs039
  32. Yun J, Kang S, Park S, Yoon H, Kim MJ, Heu S, et al. Characterization of a novel amylolytic enzyme encoded by a gene from a soil-derived metagenomic library. Appl Environ Microbiol 2004;70:7229-7235. https://doi.org/10.1128/AEM.70.12.7229-7235.2004
  33. Sharma S, Khan FG, Qazi GN. Molecular cloning and characterization of amylase from soil metagenomic library derived from Northwestern Himalayas. Appl Microbiol Biotechnol 2010;86:1821-1828. https://doi.org/10.1007/s00253-009-2404-y
  34. Liu J, Liu WD, Zhao XL, Shen WJ, Cao H, Cui ZL. Cloning and functional characterization of a novel endo-beta-1,4-glucanase gene from a soil-derived metagenomic library. Appl Microbiol Biotechnol 2011;89:1083-1092. https://doi.org/10.1007/s00253-010-2828-4
  35. Verma D, Kawarabayasi Y, Miyazaki K, Satyanarayana T. Cloning, expression and characteristics of a novel alkalistable and thermostable xylanase encoding gene (Mxyl) retrieved from compost-soil metagenome. PLoS One 2013;8:e52459. https://doi.org/10.1371/journal.pone.0052459
  36. Tao W, Lee MH, Wu J, Kim NH, Kim JC, Chung E, et al. Inactivation of chloramphenicol and florfenicol by a novel chloramphenicol hydrolase. Appl Environ Microbiol 2012;78: 6295-6301. https://doi.org/10.1128/AEM.01154-12
  37. Elend C, Schmeisser C, Leggewie C, Babiak P, Carballeira JD, Steele HL, et al. Isolation and biochemical characterization of two novel metagenome-derived esterases. Appl Environ Microbiol 2006;72:3637-3645. https://doi.org/10.1128/AEM.72.5.3637-3645.2006
  38. Hong KS, Lim HK, Chung EJ, Park EJ, Lee MH, Kim JC, et al. Selection and characterization of forest soil metagenome genes encoding lipolytic enzymes. J Microbiol Biotechnol 2007; 17:1655-1660.
  39. Lee MH, Hong KS, Malhotra S, Park JH, Hwang EC, Choi HK, et al. A new esterase EstD2 isolated from plant rhizosphere soil metagenome. Appl Microbiol Biotechnol 2010;88:1125- 1134. https://doi.org/10.1007/s00253-010-2729-6
  40. Yu EY, Kwon MA, Lee M, Oh JY, Choi JE, Lee JY, et al. Isolation and characterization of cold-active family VIII esterases from an arctic soil metagenome. Appl Microbiol Biotechnol 2011; 90:573-581. https://doi.org/10.1007/s00253-011-3132-7
  41. Faoro H, Glogauer A, Couto GH, de Souza EM, Rigo LU, Cruz LM, et al. Characterization of a new Acidobacteria-derived moderately thermostable lipase from a Brazilian Atlantic Forest soil metagenome. FEMS Microbiol Ecol 2012;81: 386-394. https://doi.org/10.1111/j.1574-6941.2012.01361.x
  42. Jiang C, Li SX, Luo FF, Jin K, Wang Q, Hao ZY, et al. Biochemical characterization of two novel beta-glucosidase genes by metagenome expression cloning. Bioresour Technol 2011;102:3272-3278. https://doi.org/10.1016/j.biortech.2010.09.114
  43. Li G, Jiang Y, Fan XJ, Liu YH. Molecular cloning and characterization of a novel beta-glucosidase with high hydrolyzing ability for soybean isoflavone glycosides and glucose-tolerance from soil metagenomic library. Bioresour Technol 2012;123: 15-22. https://doi.org/10.1016/j.biortech.2012.07.083
  44. Riaz K, Elmerich C, Moreira D, Raffoux A, Dessaux Y, Faure D. A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases. Environ Microbiol 2008; 10:560-570. https://doi.org/10.1111/j.1462-2920.2007.01475.x
  45. Schipper C, Hornung C, Bijtenhoorn P, Quitschau M, Grond S, Streit WR. Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Pseudomonas aeruginosa. Appl Environ Microbiol 2009;75:224-33. https://doi.org/10.1128/AEM.01389-08
  46. Neveu J, Regeard C, DuBow MS. Isolation and characterization of two serine proteases from metagenomic libraries of the Gobi and Death Valley deserts. Appl Microbiol Biotechnol 2011;91:635-644. https://doi.org/10.1007/s00253-011-3256-9
  47. Chen IC, Lin WD, Hsu SK, Thiruvengadam V, Hsu WH. Isolation and characterization of a novel lysine racemase from a soil metagenomic library. Appl Environ Microbiol 2009; 75:5161-5166. https://doi.org/10.1128/AEM.00074-09
  48. Ye M, Li G, Liang WQ, Liu YH. Molecular cloning and characterization of a novel metagenome-derived multicopper oxidase with alkaline laccase activity and highly soluble expression. Appl Microbiol Biotechnol 2010;87:1023-1031. https://doi.org/10.1007/s00253-010-2507-5
  49. Bijtenhoorn P, Mayerhofer H, Müller-Dieckmann J, Utpatel C, Schipper C, Hornung C, et al. A novel metagenomic shorthain dehydrogenase/reductase attenuates Pseudomonas aeruginosa biofilm formation and virulence on Caenorhabditis elegans. PLoS One 2011;6:e26278. https://doi.org/10.1371/journal.pone.0026278
  50. Brady SF, Chao CJ, Handelsman J, Clardy J. Cloning and heterologous expression of a natural product biosynthetic gene cluster from eDNA. Org Lett 2001;3:1981-1984. https://doi.org/10.1021/ol015949k
  51. Brady SF, Clardy J. Synthesis of long-chain fatty acid enol esters isolated from an environmental DNA clone. Org Lett 2003;5:121-124. https://doi.org/10.1021/ol0267681
  52. Chang FY, Brady SF. Discovery of indolotryptoline antiproliferative agents by homology-guided metagenomic screening. Proc Natl Acad Sci U S A 2013;110:2478-2483. https://doi.org/10.1073/pnas.1218073110
  53. Courtois S, Cappellano CM, Ball M, Francou FX, Normand P, Helynck G, et al. Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol 2003;69:49-55. https://doi.org/10.1128/AEM.69.1.49-55.2003
  54. Feng Z, Kim JH, Brady SF. Fluostatins produced by the heterologous expression of a TAR reassembled environmental DNA derived type II PKS gene cluster. J Am Chem Soc 2010; 132:11902-11903. https://doi.org/10.1021/ja104550p
  55. Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles MR, Rondon MR, et al. Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 2002;68:4301-4306. https://doi.org/10.1128/AEM.68.9.4301-4306.2002
  56. King RW, Bauer JD, Brady SF. An environmental DNA-derived type II polyketide biosynthetic pathway encodes the biosynthesis of the pentacyclic polyketide erdacin. Angew Chem Int Ed Engl 2009;48:6257-6261. https://doi.org/10.1002/anie.200901209
  57. Kim JS, Lim HK, Lee MH, Park JH, Hwang EC, Moon BJ, et al. Production of porphyrin intermediates in Escherichia coli carrying soil metagenomic genes. FEMS Microbiol Lett 2009; 295:42-49. https://doi.org/10.1111/j.1574-6968.2009.01577.x
  58. Owen JG, Robins KJ, Parachin NS, Ackerley DF. A functional screen for recovery of 4'-phosphopantetheinyl transferase and associated natural product biosynthesis genes from metagenome libraries. Environ Microbiol 2012;14:1198-1209. https://doi.org/10.1111/j.1462-2920.2012.02699.x

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