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Nat Microbiol. 2019 Feb;4(2):352-361. doi: 10.1038/s41564-018-0312-6. Epub 2018 Dec 3.

Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing.

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Department of Microbiology, Ohio State University, Columbus, OH, USA.
Joint Genome Institute, Walnut Creek, CA, USA.
Environmental Sciences Graduate Program, Ohio State University, Columbus, OH, USA.
School of Earth Sciences, Ohio State University, Columbus, OH, USA.
Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, USA.
Molecular and Cellular Imaging Center, Ohio State University, Wooster, OH, USA.
Department of Civil, Environmental, and Geodetic Engineering, Ohio State University, Columbus, OH, USA.
Department of Civil and Environmental Engineering, University of New Hampshire, Durham, NH, USA.
Dow Microbial Control, Collegeville, PA, USA.
Dow Microbial Control, Houston, TX, USA.
Department of Microbiology, Ohio State University, Columbus, OH, USA.
School of Earth Sciences, Ohio State University, Columbus, OH, USA.


The deep terrestrial biosphere harbours a substantial fraction of Earth's biomass and remains understudied compared with other ecosystems. Deep biosphere life primarily consists of bacteria and archaea, yet knowledge of their co-occurring viruses is poor. Here, we temporally catalogued viral diversity from five deep terrestrial subsurface locations (hydraulically fractured wells), examined virus-host interaction dynamics and experimentally assessed metabolites from cell lysis to better understand viral roles in this ecosystem. We uncovered high viral diversity, rivalling that of peatland soil ecosystems, despite low host diversity. Many viral operational taxonomic units were predicted to infect Halanaerobium, the dominant microorganism in these ecosystems. Examination of clustered regularly interspaced short palindromic repeats-CRISPR-associated proteins (CRISPR-Cas) spacers elucidated lineage-specific virus-host dynamics suggesting active in situ viral predation of Halanaerobium. These dynamics indicate repeated viral encounters and changing viral host range across temporally and geographically distinct shale formations. Laboratory experiments showed that prophage-induced Halanaerobium lysis releases intracellular metabolites that can sustain key fermentative metabolisms, supporting the persistence of microorganisms in this ecosystem. Together, these findings suggest that diverse and active viral populations play critical roles in driving strain-level microbial community development and resource turnover within this deep terrestrial subsurface ecosystem.

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