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High proportions of bacteria are culturable across major biomes

The ISME Journal (2019) | Download Citation

Abstract

The paradigm that only 1% of microbes are culturable has had a profound impact on our understanding of microbial ecology and is still a major motivation for mostly using molecular tools to characterize microbial communities. However, this point is often expressed vaguely, suggesting that some scientists have different interpretations of the paradigm. In addition, there have been substantial advances in cultivation techniques suggesting that this paradigm may no longer be correct. To quantify bacterial culturability across six major biomes, I found that the median 16S rRNA similarity of bacteria to known cultured relatives was 97.3 ± 2.3% (s.d.). Furthermore, 52.0 ± 24% of sequences and 34.9 ± 23% of taxa (defined as >97% similar) had a closely related cultured relative. Thus, many cells and taxa across environments are culturable with known techniques, suggesting that the 1% paradigm is no longer correct.

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References

  1. 1.

    Brock TD. The study of microorganisms in situ: progress and problems. Symp Soc Gen Microbiol. 1987;41:1–17.

  2. 2.

    Staley JT, Konopka A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol. 1985;39:321–46.

  3. 3.

    Torsvik V, Øvreås L. Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol. 2002;5:240–5.

  4. 4.

    Amann RI, Ludwig W, Schleifer K-H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995;59:143–69.

  5. 5.

    Giovannoni S, Stingl U. The importance of culturing bacterioplankton in the ‘omics’ age. Nat Rev Microbiol. 2007;5:820–6.

  6. 6.

    Joseph SJ, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH. Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol. 2003;69:7210–5.

  7. 7.

    Kaeberlein T, Lewis K, Epstein SS. Isolating ‘uncultivable’ microorganisms in pure culture in a simulated natural environment. Science. 2002;296:1127–9.

  8. 8.

    Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014;42. https://doi.org/10.1093/nar/gkt1244.

  9. 9.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

  10. 10.

    Rosselló-Móra R, Amann R. Past and future species definitions for Bacteria and Archaea. Syst. Appl. Microbiol. 2015;38:209–216.

  11. 11.

    Van Der Star WRL, Miclea AI, Van Dongen UGJM, Muyzer G, Picioreanu C, Van Loosdrecht MCM. The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng. 2008;101:286–94.

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Acknowledgements

I would like to thank Alyse Larkin, Sydney Glassman, and Jennifer Martiny for many helpful comments and acknowledge support for this work from NSF (OCE-1559002, OCE-1848576, and DEB-1457160) and the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research (BER), under award number (DE-SC0016410).

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  1. Department of Earth System Science, University of California, Irvine, CA, 92697, USA

    • Adam C. Martiny
  2. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA

    • Adam C. Martiny

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The author declare that he has no conflict of interest.

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Correspondence to Adam C. Martiny.

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DOI

https://doi.org/10.1038/s41396-019-0410-3