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A virus or more in (nearly) every cell: ubiquitous networks of virus–host interactions in extreme environments

The ISME Journalvolume 12pages17061714 (2018) | Download Citation

Abstract

The application of viral and cellular metagenomics to natural environments has expanded our understanding of the structure, functioning, and diversity of microbial and viral communities. The high diversity of many communities, e.g., soils, surface ocean waters, and animal-associated microbiomes, make it difficult to establish virus-host associations at the single cell (rather than population) level, assign cellular hosts, or determine the extent of viral host range from metagenomics studies alone. Here, we combine single-cell sequencing with environmental metagenomics to characterize the structure of virus–host associations in a Yellowstone National Park (YNP) hot spring microbial community. Leveraging the relatively low diversity of the YNP environment, we are able to overlay evidence at the single-cell level with contextualized viral and cellular community structure. Combining evidence from hexanucelotide analysis, single cell read mapping, network-based analytics, and CRISPR-based inference, we conservatively estimate that >60% of cells contain at least one virus type and a majority of these cells contain two or more virus types. Of the detected virus types, nearly 50% were found in more than 2 cellular clades, indicative of a broad host range. The new lens provided by the combination of metaviromics and single-cell genomics reveals a network of virus–host interactions in extreme environments, provides evidence that extensive virus–host associations are common, and further expands the unseen impact of viruses on cellular life.

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Acknowledgements

We thank Jennifer Wirth and Ross Hartman for critical review of this work, and three reviewers for their feedback on the manuscript. This study was supported by National Science Foundation grant DEB-4W4596 to RJW, JSW, and MJY. This research was conducted in Yellowstone National Park under the conditions of permit YELL-2013-SCI-5090.

Author contributions

RJW, JSW, and MJY conceived the study. JHMM, RS, SP, and SD performed the experiments and analysis. JHMM, SP, RJW, JSW, and MY prepared the manuscript with input from all authors.

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Author notes

  1. These authors contributed equally: Jacob H. Munson-McGee and Shengyun Peng.

Affiliations

  1. Department of Microbiology and Immunology, Montana State University, Bozeman, Montana, USA

    • Jacob H. Munson-McGee
    •  & Mark J. Young
  2. School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA

    • Shengyun Peng
    •  & Joshua S. Weitz
  3. Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

    • Samantha Dewerff
    •  & Rachel J. Whitaker
  4. Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine, USA

    • Ramunas Stepanauskas
  5. School of Physics, Georgia Institute of Technology, Atlanta, Georgia, USA

    • Joshua S. Weitz
  6. Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, USA

    • Mark J. Young

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Conflict of interest

The authors declare that they have no conflict of interest.

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Correspondence to Mark J. Young.

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DOI

https://doi.org/10.1038/s41396-018-0071-7