Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface
Abstract
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 terrestrialmore »
- Authors:
-
[1];
[5];
- 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)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); West Virginia Univ., Morgantown, WV (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Energy Technology Laboratory (NETL); Natural Environment Research Council Research Fellowship; National Science Foundation (NSF)
- OSTI Identifier:
- 1626160
- Grant/Contract Number:
- AC02-05CH11231; FE0024297; NE/R013462/1; 1342701; EAR-1847684
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mSphere
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 6; Journal ID: ISSN 2379-5042
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; microbiology; glycoside hydrolases; viruse; shale; hypersaline; hydraulic fracturing
Citation Formats
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., and Suen, Garret. Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface. United States: N. p., 2019.
Web. doi:10.1128/msphere.00613-19.
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. Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface. United States. https://doi.org/10.1128/msphere.00613-19
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., and Suen, Garret. Wed .
"Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface". United States. https://doi.org/10.1128/msphere.00613-19. https://www.osti.gov/servlets/purl/1626160.
@article{osti_1626160,
title = {Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface},
author = {Nixon, Sophie L. and Daly, Rebecca A. and Borton, Mikayla A. and Solden, Lindsey M. and Welch, Susan A. and Cole, David R. and Mouser, Paula J. and Wilkins, Michael J. and Wrighton, Kelly C. and Suen, Garret},
abstractNote = {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.},
doi = {10.1128/msphere.00613-19},
journal = {mSphere},
number = 6,
volume = 4,
place = {United States},
year = {2019},
month = {12}
}
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