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

Abstract

Bacteria of the phylumVerrucomicrobiaare prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members ofVerrucomicrobiaare important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, theVerrucomicrobiaare underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of theVerrucomicrobiaphylum by describing a novel genus, “CandidatusMarcellius,” belonging to the orderOpitutales. “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 theVerrucomicrobiahas 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 theVerrucomicrobiaphylum, we performed a comparative genomic analysis of 31 publicly available, nearly completeVerrucomicrobiagenomes. Our genomic findings extend the environmental distribution of theVerrucomicrobia2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of theVerrucomicrobia, including the capacity to degrade hemicellulose and tomore » adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum. IMPORTANCETheVerrucomicrobiaphylum of bacteria is widespread in many different ecosystems; however, its role in microbial communities remains poorly understood.Verrucomicrobiaare often low-abundance community members, yet previous research suggests they play a major role in organic carbon degradation. WhileVerrucomicrobiaremain poorly represented in culture collections, numerous genomes have been reconstructed from metagenomic data sets in recent years. The study of genomes from across the phylum allows for an extensive assessment of their potential ecosystem roles. The significance of this work is (i) the recovery of a novel genus ofVerrucomicrobiafrom 2.3 km in the subsurface with the ability to withstand the extreme conditions that characterize this environment, and (ii) the most extensive assessment of ecophysiological traits encoded by Verrucomicrobia genomes to date. We show that members of this phylum are specialist organic polymer degraders that can withstand a wider range of environmental conditions than previously thought.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [4];  [4]; ORCiD logo [5];  [2];  [2];
  1. Department of Earth and Environmental Sciences, University of Manchester, Manchester, United Kingdom
  2. Soil and Crop Sciences, Colorado State University, Fort Collins, Colorado, USA
  3. Centre for Microbial Pathogenesis, The Research Institute at Nationwide Children’s Hospital, Columbus, Ohio, USA
  4. School of Earth Sciences, The Ohio State University, Columbus, Ohio, USA
  5. College of Engineering and Physical Sciences, University of New Hampshire, Durham, New Hampshire, USA
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 Dimensions of Biodiversity
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. 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., & 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 phylumVerrucomicrobiaare prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members ofVerrucomicrobiaare important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, theVerrucomicrobiaare underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of theVerrucomicrobiaphylum by describing a novel genus, “CandidatusMarcellius,” belonging to the orderOpitutales. “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 theVerrucomicrobiahas 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 theVerrucomicrobiaphylum, we performed a comparative genomic analysis of 31 publicly available, nearly completeVerrucomicrobiagenomes. Our genomic findings extend the environmental distribution of theVerrucomicrobia2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of theVerrucomicrobia, 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. IMPORTANCETheVerrucomicrobiaphylum of bacteria is widespread in many different ecosystems; however, its role in microbial communities remains poorly understood.Verrucomicrobiaare often low-abundance community members, yet previous research suggests they play a major role in organic carbon degradation. WhileVerrucomicrobiaremain poorly represented in culture collections, numerous genomes have been reconstructed from metagenomic data sets in recent years. The study of genomes from across the phylum allows for an extensive assessment of their potential ecosystem roles. The significance of this work is (i) the recovery of a novel genus ofVerrucomicrobiafrom 2.3 km in the subsurface with the ability to withstand the extreme conditions that characterize this environment, and (ii) the most extensive assessment of ecophysiological traits encoded by Verrucomicrobia genomes to date. We show that members of this phylum are specialist organic polymer degraders that can withstand a wider range of environmental conditions than previously thought.},
doi = {10.1128/msphere.00613-19},
journal = {mSphere},
number = 6,
volume = 4,
place = {United States},
year = {2019},
month = {12}
}

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