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Impact of single-cell genomics and metagenomics on the emerging view of extremophile “microbial dark matter”

  • Special Issue: Review
  • 10th International Congress on Extremophiles
  • Published:
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Abstract

Despite >130 years of microbial cultivation studies, many microorganisms remain resistant to traditional cultivation approaches, including numerous candidate phyla of bacteria and archaea. Unraveling the mysteries of these candidate phyla is a grand challenge in microbiology and is especially important in habitats where they are abundant, including some extreme environments and low-energy ecosystems. Over the past decade, parallel advances in DNA amplification, DNA sequencing and computing have enabled rapid progress on this problem, particularly through metagenomics and single-cell genomics. Although each approach suffers limitations, metagenomics and single-cell genomics are particularly powerful when combined synergistically. Studies focused on extreme environments have revealed the first substantial genomic information for several candidate phyla, encompassing putative acidophiles (Parvarchaeota), halophiles (Nanohaloarchaeota), thermophiles (Acetothermia, Aigarchaeota, Atribacteria, Calescamantes, Korarchaeota, and Fervidibacteria), and piezophiles (Gracilibacteria). These data have enabled insights into the biology of these organisms, including catabolic and anabolic potential, molecular adaptations to life in extreme environments, unique genomic features such as stop codon reassignments, and predictions about cell ultrastructure. In addition, the rapid expansion of genomic coverage enabled by these studies continues to yield insights into the early diversification of microbial lineages and the relationships within and between the phyla of Bacteria and Archaea. In the next 5 years, the genomic foliage within the tree of life will continue to grow and the study of yet-uncultivated candidate phyla will firmly transition into the post-genomic era.

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Abbreviations

AMD:

Acid mine drainage

FACS:

Fluorescence-activated cell sorting

GEBA:

Genomic encyclopedia of bacteria and archaea

MDA:

Multiple displacement amplification

MDM:

“Microbial dark matter”

SAG:

Single amplified genome

SSU rRNA:

Small subunit ribosomal RNA

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Acknowledgments

This work was supported by NASA Exobiology grant EXO-NNX11AR78G; U.S. National Science Foundation grant OISE 0968421; U.S. Department of Energy (DOE) grant DE-EE-0000716; and the Joint Genome Institute (CSP-182), supported by the Office of Science of the U.S. DOE under Contract No. DE-AC02-05CH11231. B. P. H. acknowledges generous support from Greg Fullmer through the UNLV Foundation.

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Authors and Affiliations

  1. School of Life Sciences, University of Nevada Las Vegas, 4004, 4505 Maryland Parkway, Las Vegas, NV, 89154-4004, USA

    Brian P. Hedlund, Jeremy A. Dodsworth & Senthil K. Murugapiran

  2. DOE Joint Genome Institute, Walnut Creek, CA, 94598, USA

    Christian Rinke & Tanja Woyke

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  1. Brian P. Hedlund
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  2. Jeremy A. Dodsworth
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  3. Senthil K. Murugapiran
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  4. Christian Rinke
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  5. Tanja Woyke
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Correspondence to Brian P. Hedlund.

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Communicated by H. Santos.

This article is part of a special issue based on the 10th International Congress on Extremophiles held in Saint Petersburg, Russia, September 7-11, 2014.

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Hedlund, B.P., Dodsworth, J.A., Murugapiran, S.K. et al. Impact of single-cell genomics and metagenomics on the emerging view of extremophile “microbial dark matter”. Extremophiles 18, 865–875 (2014). https://doi.org/10.1007/s00792-014-0664-7

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