Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Microbial cultivation and the role of microbial resource centers in the omics era

Abstract

Despite tremendous advances in microbial ecology over the past two decades, traditional cultivation methods have failed to grow ecologically more relevant microorganisms in the laboratory, leading to a predominance of weed-like species in the world’s culture collections. In this review, we highlight the gap between culture-based and culture-independent methods of microbial diversity analysis, especially in investigations of slow growers, oligotrophs, and fastidious and recalcitrant microorganisms. Furthermore, we emphasize the importance of microbial cultivation and the acquisition of the cultivation-based phenotypic data for the testing of hypotheses arising from genomics and proteomics approaches. Technical difficulties in cultivating novel microorganisms and how modern approaches have helped to overcome these limitations are highlighted. After cultivation, adequate preservation without changes in genotypic and phenotypic features of these microorganisms is necessary for future research and training. Hence, the contribution of microbial resource centers in the handling, preservation, and distribution of this novel diversity is discussed. Finally, we explore the concept of microbial patenting and requisite guidelines of the “Budapest Treaty” for establishment of an International Depositary Authority.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13:583–594

  2. Amann R (2000) Who is out there? Microbial aspects of diversity. Syst Appl Microbiol 23:1–8

  3. Arrigo K (2005) Marine microorganisms and global nutrient cycles. Nature 437:349–355

  4. Bent SJ, Forney LJ (2008) The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J 2:689–695

  5. Bouzas TD, Barros-Velazquez J, Villa TG (2006) Industrial applications of hyperthermophilic enzymes: a review. Prot Pept Lett 13:445–451

  6. Bruns A, Cypionka H, Overmann J (2002) Cyclic AMP and acyl homoserine lactones increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea. Appl Environ Microbiol 68:3978–3987

  7. Cardenas E, Tiedje JM (2008) New tools for discovering and characterizing microbial diversity. Curr Opin Biotechnol 19:544–549

  8. Challis G, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 2:14555–14561

  9. Chen GQ, Wu Q (2005) The application of polyhydroxyalkanoates as tissue engineering materials. Biomaterials 26:6565–6578

  10. Coenye T, Vandamme P (2004) Bacterial whole-genome sequences: minimal information and strain availability. Microbiology 150:2017–2018

  11. Colwell RR (1997) Microbial diversity: the importance of exploration and conservation. J Ind Microbiol Biotechnol 18:302–307

  12. Connon SA, Giovannoni SJ (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new many isolates. Appl Environ Microbiol 68:3878–3885

  13. Cypess R (2003) Biological resource centers: from concept to reality. American Type Culture Collection, Manassas, VA.

  14. Davis KE, Joseph SJ, Janssen PH (2005) Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria. Appl Environ Microb 71:826–834

  15. Donachie SP, Foster JS, Brown MV (2007) Culture clash: challenging the dogma of microbial diversity. ISME J 1:97–99

  16. Dorit R (2008) All things small and great. Am Sci 96:284–286

  17. Emerson D, Wilson W (2009) Giving microbial diversity a home. Nat Rev Microbiol 7:758

  18. Endy D (2005) Foundations for engineering biology. Nature 438:449–453

  19. Ferrari B, Gillings MR (2009) Cultivation of fastidious bacteria by viability staining and micromanipulation in a soil substrate membrane system. Appl Environ Microbiol 75:3352–3354

  20. Ferrari B, Winsley T, Gillings M, Binnerup S (2008) Cultivating previously uncultured soil bacteria using a soil substrate membrane system. Nat Protoc 3:1261–1269

  21. Field D, Hughes J (2005) Cataloguing our current genome collection. Microbiology 151:1016–1019

  22. Fritze D (1994) Patent aspects of the convention at the microbial level. In: Kirsop B, Hawksworth DL (eds) The biodiversity of micro-organisms and the role of microbial resource centres. World Federation of Culture Collections, Braunschweig, pp 37–43

  23. Frohlich J, Konig H (2000) New techniques for isolation of single prokaryotic cells. FEMS Microbiol Rev 24:567–572

  24. Fry J (2000) Bacterial diversity and unculturables. Microbiol Today 27:186–188

  25. Gest H (2001) Evolution of knowledge encapsulated in scientific definitions. Persp Biol Med 44:556–564

  26. Gest H (2008; posting date). The modern myth of “unculturable” bacteria/scotoma of contemporary microbiology. http://hdl.handle.net/2022/3149

  27. Giovannoni S, Stingl U (2007) The importance of culturing bacterioplankton in the “omics” age. Nat Rev Microbiol 5:820–826

  28. Giovannoni SJ, Foster RA, Rappe MS, Epstein S (2007) New cultivation strategies bring more microbial plankton species into the laboratory. Oceanography 20:62–69

  29. Gírio FM, Fonseca C, Carvalheiro F, Duarte LC, Marques S, Bogel-Łukasik R (2010) Hemicelluloses for fuel ethanol: a review. Bioresour Technol 13:4775–4800

  30. Gordon RF, Stein MA, Diedrich DI (1993) Heat shock induced axenic growth of Bdellovibrio bacteriovorus. J Bacteriol 175:2157–2161

  31. Green SJ, Prakash O, Akob DM, Gihring TM, Jardin P, Watson DB, Kostka JE (2010) Denitrifying bacteria isolated from terrestrial subsurface sediment exposed to mixed contamination. Appl Environ Microbiol 76:3244–3254

  32. Gupta R, Beg QK, Lorenz P (2002) Bacterial alkaline proteases: molecular approaches and industrial applications. Appl Microbiol Biotechnol 59:15–32

  33. Hahn MW, Stadler P, Wu QL, Pockl M (2004) The filtration-acclimatization method for isolation of an important fraction of the not readily cultivable bacteria. J Microbiol Meth 57:379–390

  34. Heylen K, Hoefman S, Vekeman B, Peiren J, De Vos P (2012) Safeguarding bacterial resources promotes biotechnological innovation. Appl Microbiol Biotechnol 94:565–574

  35. Huber R, Burggraf S, Mayer T, Barns SM, Rossnagel P, Stetter KO (1995) Isolation of a hyperthermophilic archaeum predicted by in situ RNA analysis. Nature 376:57–58

  36. Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO (2002) A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nat 417:27–28

  37. Hughes DT, Sperandio V (2008) Inter-kingdom signaling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120

  38. Ingham CJ, Sprenkels A, Bomer J, Molenaar D, van den Berg A, van Hylckama Vlieg JE, de Vos WM (2007) The micro-Petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc Natl Acad Sci U S A 104:18217–18222

  39. Janssens D, Arahal DR, Bizet C, Garay E (2010) The role of public biological resource centers in providing a basic infrastructure for microbial research. Res Microbiol 161:422–429

  40. Joseph S, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH (2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol 69:7210–7215

  41. Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1227–1229

  42. Kamagata Y, Fulthorpe RR, Tamura K, Takami H, Forney LJ, Tiedje JM (1997) Pristine environments harbor a new group of oligotrophic 2,4-dichlorophenoxyacetic acid-degrading bacteria. Appl Environ Microbiol 63:2266–2272

  43. Kamagata Y, Tamaki H (2005) Cultivation of uncultured fastidious microbes. Microbes Environ 20:85–91

  44. Keller M, Zengler K (2004) Tapping into microbial diversity. Nat Rev Microbiol 2:141–150

  45. Kelley J, Smith D (1997) Depositing micro-organisms as part of the patenting process. Ballantyne Ross Ltd, London

  46. Kim JJ, Kim HN, Masui R, Kuramitsu S, Seo JH, Kim K, Sung MH (2008) Isolation of uncultivable anaerobic thermophiles of the family Clostridiaceae requiring growth-supporting factors. J Microbiol Biotechn 18:611–615

  47. Köpke B, Wilms R, Engelen B, Cypionka H, Sass H (2005) Microbial diversity in coastal subsurface sediments: a cultivation approach using various electron acceptors and substrate gradients. Appl Environ Microbiol 71:7819–7830

  48. Kostka JE, Prakash O, Overholt W, Green S, Freyer G, Canion A, Delgardio J, Norton N, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol 77:7962–7797

  49. Kuske C, Ticknor LO, Miller ME, Dunbar JM, Davis JA, Barns SM, Belnap J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68:1854–1863

  50. Labeda DP, Oren A (2008) International Committee on Systematics of Prokaryotes; XIth International (IUMS) Congress of Microbiology and Applied Bacteriology, Minutes of the meetings, 23, 24, 26 and 28 July 2005, San Francisco, CA, USA. Int J Syst Evol Microbiol (58):1746–1752

  51. Lal R, Pandey G, Sharma P, Kumari K, Malhotra S, Pandey R, Raina V, Kohler HP, Holliger C, Jackson C, Oakeshott JG (2010) Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol Mol Biol Rev 74:58–80

  52. Leadbetter JR (2003) Cultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Curr Opin Microbiol 6:274–281

  53. Lewis N, Nagarajan H, Palsson BO (2012) Constraining the metabolic genotype-phenotype relationship using a phylogeny of in silico methods. Nat Rev Microbiol 10:291–305

  54. Lomax AR, Calder PC (2009) Prebiotics, immune function, infection and inflammation: a review of the evidence. Br J Nutr 101:633–658

  55. Lovley DR (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4:497–508

  56. Lupp C (2007) Host–microbes interactions. Nature 449:830

  57. Malik KA, Claus D (1987) Bacterial culture collections: their importance to biotechnology and microbiology. Biotechnol Genet Eng Rev 5:137–197

  58. Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31–46

  59. Morales SE, Holben WE (2011) Linking bacterial identities and ecosystem processes: can ‘omic’ analyses be more than the sum of their parts? FEMS Microbiol Ecol 75:2–16

  60. Nichols D, Lewis K, Orjala J, Mo S, Ortenberg R, O’Connor P, Zhao C, Vouros P, Kaeberlein T, Epstein SS (2008) Short peptide induces an ‘uncultivable’ microorganism to grow in vitro. Appl Environ Microb 74:4889–4897

  61. Ogawa J, Shimizu S (2002) Industrial microbial enzymes: their discovery by screening and use in large-scale production of useful chemicals in Japan. Curr Opin Biotechno 13:367–375

  62. Ohno M, Okano I, Watsuji T, Kakinuma T, Ueda K, Beppu T (1999) Establishing the independent culture of a strictly symbiotic bacterium Symbiobacterium thermophilum from its supporting Bacillus strain. Biosci Biotechnol Biochem 63:1083–1090

  63. Overmann J (2006) Principal of enrichment, isolation, cultivation and preservation of prokaryotes. Prokaryotes 1:80–136

  64. Palleroni NJ (1997) Prokaryotic diversity and the importance of culturing. Antonie Van Leeuwenhoek 72:3–19

  65. Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic JM (2009) Pyrosequencing and microbial identification. Clin Chem 5:856–866

  66. Pham VH, Kim J (2012) Cultivation of unculturable soil bacteria. Trends Biotechnol 30:475–484

  67. Prakash O, Nimonkar Y, Shouche YS (2012) Practice and prospects of microbial preservation. FEMS Microbiol Lett. doi:10:1111/1574-6968

  68. Rappe MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633

  69. Rawlings DE, Silver S (1995) Mining with microbes. Nat Biotechnol 13:773–778

  70. Saeki K, Ozaki K, Kobayashi T, Ito S (2007) Detergent alkaline proteases: enzymatic properties, genes, and crystal structures. J Biosci Bioeng 103:501–508

  71. Sekar S, Kandavel D (2004) The future of patent deposition of microorganisms? Trends Biotechnol 22:213–218

  72. Senni K, Pereira J, Gueniche F, Delbarre-Ladrat C, Sinquin C, Ratiskol J, Godeau G, Fischer AM, Helley D, Sylvia CJ (2011) Marine polysaccharides: a source of bioactive molecules for cell therapy and tissue engineering. Mar Drugs 9:1664–1681

  73. Singh BK, Richard D, Smith BP, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790

  74. Song J, Oh HM, Cho JC (2009) Improved culturability of SAR11 strains in dilution-to-extinction culturing from the East Sea, West Pacific Ocean. FEMS Microbiol Lett 295:141–147

  75. Stackebrandt E (2011) Towards a strategy to enhance access to microbial diversity. Int J Syst Evol Microbiol 61:479–481

  76. Stern S (2004) Biological resource centers: knowledge hubs for the life sciences. Brookings Institution Press, Washington (DC)

  77. Stevenson BS, Eichorst SA, Wertz JT, Schmidt TM, Breznak JA (2004) New strategies for cultivation and detection of previously uncultured microbe. Appl Environ Microbiol 70:4748–4755

  78. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160

  79. Tripp HJ, Kitner JB, Schwalbach MS, Dacey JW, Wilhelm LJ, Giovannoni SJ (2008) SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452:741–744

  80. Tyson GW, Banfield JF (2005) Cultivating the uncultivated: a community genomics perspective. Trends Microbiol 9:411–415

  81. Unsworth LD, van der Oost J, Koutsopoulos S (2007) Hyperthermophilic enzymes—stability, activity and implementation strategies for high temperature applications. FEBS J 274:4044–4056

  82. Verlindin RA, Hill DJ, Kenward MA, Williams CD, Radecka I (2007) Bacterial synthesis of biodegradable polyhydroxyalkanoates. J Appl Microbiol 102:1437–1449

  83. Walker JCG (1980) The oxygen cycle in the natural environment and the biogeochemical cycles. Springer, Berlin

  84. Ward N, Eisen J, Fraser C, Stackebrandt E (2001) Sequenced strains must be saved from extinction. Nature 414:148

  85. Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95:6578–6583

  86. Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284

  87. Zengler K (2009) Central role of the cell in microbial ecology. Microbiol Mol Biol Rev 73:712–729

  88. Zengler K, Palsson BO (2012) A road map for the development of community systems (CoSy) biology. Nat Rev Microbiol 10:366–372

  89. Zengler K, Toledo C, Rappe M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proc Natl Acad Sci U S A 99:15681–15686

Download references

Acknowledgments

This work was supported from the grant no. BT/PR/0054/NDB/52/94/2007 funded by Department of Biotechnology (DBT), Government of India, under the project “Establishment of microbial culture collection.” We are grateful to our colleagues, especially Kiran N. Mahale, and anonymous reviewers for critically reading the manuscript and providing valuable critics and comments for its improvement.

Author information

Correspondence to Om Prakash.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Prakash, O., Shouche, Y., Jangid, K. et al. Microbial cultivation and the role of microbial resource centers in the omics era. Appl Microbiol Biotechnol 97, 51–62 (2013). https://doi.org/10.1007/s00253-012-4533-y

Download citation

Keywords

  • Cultivation
  • Preservation
  • Microbial resource centers
  • Budapest Treaty