Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface

Nixon, Sophie L.; Daly, Rebecca A.; Borton, Mikayla A.; Solden, Lindsey M.; Welch, Susan A.; Cole, David R.; Mouser, Paula J.; Wilkins, Michael J.; Wrighton, Kelly C.; Suen, Garret

doi:10.1128/msphere.00613-19

Title: Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface

Journal Article · Wed Dec 18 00:00:00 EST 2019 · mSphere

DOI:https://doi.org/10.1128/msphere.00613-19· OSTI ID:1626160

^[1]; Daly, Rebecca A. ^[2]; Borton, Mikayla A. ^[2]; Solden, Lindsey M. ^[3]; Welch, Susan A. ^[4]; Cole, David R. ^[4];

^[5]; Wilkins, Michael J. ^[2]; Wrighton, Kelly C. ^[2]; Suen, Garret ^[6]

Univ. of Manchester (United Kingdom)
Colorado State Univ., Fort Collins, CO (United States)
The Research Institute at Nationwide Children's Hospital, Columbus, OH (United States)
The Ohio State Univ., Columbus, OH (United States)
Univ. of New Hampshire, Durham, NH (United States)
Univ. of Wisconsin, Madison, WI (United States)

Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by describing a novel genus, “Candidatus Marcellius,” belonging to the order Opitutales. “Ca. Marcellius” was recovered from a shale-derived produced fluid metagenome collected 313 days after hydraulic fracturing, the deepest environment from which a member of the Verrucomicrobia has been recovered to date. We uncover genomic attributes that may explain the capacity of this organism to inhabit a shale gas well, including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of the Verrucomicrobia, including the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); West Virginia Univ., Morgantown, WV (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Energy Technology Laboratory (NETL); Natural Environment Research Council Research Fellowship; National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; FE0024297; NE/R013462/1; 1342701; EAR-1847684

OSTI ID:: 1626160

Journal Information:: mSphere, Vol. 4, Issue 6; ISSN 2379-5042

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 23 works

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59 BASIC BIOLOGICAL SCIENCES
microbiology
glycoside hydrolases
viruse
shale
hypersaline
hydraulic fracturing

Title: Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface

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