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Title: Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing

Abstract

ABSTRACT Rapidly thawing permafrost harbors ∼30 to 50% of global soil carbon, and the fate of this carbon remains unknown. Microorganisms will play a central role in its fate, and their viruses could modulate that impact via induced mortality and metabolic controls. Because of the challenges of recovering viruses from soils, little is known about soil viruses or their role(s) in microbial biogeochemical cycling. Here, we describe 53 viral populations (viral operational taxonomic units [vOTUs]) recovered from seven quantitatively derived (i.e., not multiple-displacement-amplified) viral-particle metagenomes (viromes) along a permafrost thaw gradient at the Stordalen Mire field site in northern Sweden. Only 15% of these vOTUs had genetic similarity to publicly available viruses in the RefSeq database, and ∼30% of the genes could be annotated, supporting the concept of soils as reservoirs of substantial undescribed viral genetic diversity. The vOTUs exhibited distinct ecology, with different distributions along the thaw gradient habitats, and a shift from soil-virus-like assemblages in the dry palsas to aquatic-virus-like assemblages in the inundated fen. Seventeen vOTUs were linked to microbial hosts ( in silico ), implicating viruses in infecting abundant microbial lineages from Acidobacteria , Verrucomicrobia , and Deltaproteobacteria , including those encoding key biogeochemical functions suchmore » as organic matter degradation. Thirty auxiliary metabolic genes (AMGs) were identified and suggested virus-mediated modulation of central carbon metabolism, soil organic matter degradation, polysaccharide binding, and regulation of sporulation. Together, these findings suggest that these soil viruses have distinct ecology, impact host-mediated biogeochemistry, and likely impact ecosystem function in the rapidly changing Arctic. IMPORTANCE This work is part of a 10-year project to examine thawing permafrost peatlands and is the first virome-particle-based approach to characterize viruses in these systems. This method yielded >2-fold-more viral populations (vOTUs) per gigabase of metagenome than vOTUs derived from bulk-soil metagenomes from the same site (J. B. Emerson, S. Roux, J. R. Brum, B. Bolduc, et al., Nat Microbiol 3:870–880, 2018, https://doi.org/10.1038/s41564-018-0190-y). We compared the ecology of the recovered vOTUs along a permafrost thaw gradient and found (i) habitat specificity, (ii) a shift in viral community identity from soil-like to aquatic-like viruses, (iii) infection of dominant microbial hosts, and (iv) carriage of host metabolic genes. These vOTUs can impact ecosystem carbon processing via top-down (inferred from lysing dominant microbial hosts) and bottom-up (inferred from carriage of auxiliary metabolic genes) controls. This work serves as a foundation which future studies can build upon to increase our understanding of the soil virosphere and how viruses affect soil ecosystem services.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1475081
Alternate Identifier(s):
OSTI ID: 1506353
Grant/Contract Number:  
SC0004632; SC0010580; SC0016440; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Name: mSystems Journal Volume: 3 Journal Issue: 5; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Trubl, Gareth, Jang, Ho Bin, Roux, Simon, Emerson, Joanne B., Solonenko, Natalie, Vik, Dean R., Solden, Lindsey, Ellenbogen, Jared, Runyon, Alexander T., Bolduc, Benjamin, Woodcroft, Ben J., Saleska, Scott R., Tyson, Gene W., Wrighton, Kelly C., Sullivan, Matthew B., Rich, Virginia I., and Bordenstein, ed., Seth. Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing. United States: N. p., 2018. Web. doi:10.1128/mSystems.00076-18.
Trubl, Gareth, Jang, Ho Bin, Roux, Simon, Emerson, Joanne B., Solonenko, Natalie, Vik, Dean R., Solden, Lindsey, Ellenbogen, Jared, Runyon, Alexander T., Bolduc, Benjamin, Woodcroft, Ben J., Saleska, Scott R., Tyson, Gene W., Wrighton, Kelly C., Sullivan, Matthew B., Rich, Virginia I., & Bordenstein, ed., Seth. Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing. United States. https://doi.org/10.1128/mSystems.00076-18
Trubl, Gareth, Jang, Ho Bin, Roux, Simon, Emerson, Joanne B., Solonenko, Natalie, Vik, Dean R., Solden, Lindsey, Ellenbogen, Jared, Runyon, Alexander T., Bolduc, Benjamin, Woodcroft, Ben J., Saleska, Scott R., Tyson, Gene W., Wrighton, Kelly C., Sullivan, Matthew B., Rich, Virginia I., and Bordenstein, ed., Seth. Tue . "Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing". United States. https://doi.org/10.1128/mSystems.00076-18.
@article{osti_1475081,
title = {Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing},
author = {Trubl, Gareth and Jang, Ho Bin and Roux, Simon and Emerson, Joanne B. and Solonenko, Natalie and Vik, Dean R. and Solden, Lindsey and Ellenbogen, Jared and Runyon, Alexander T. and Bolduc, Benjamin and Woodcroft, Ben J. and Saleska, Scott R. and Tyson, Gene W. and Wrighton, Kelly C. and Sullivan, Matthew B. and Rich, Virginia I. and Bordenstein, ed., Seth},
abstractNote = {ABSTRACT Rapidly thawing permafrost harbors ∼30 to 50% of global soil carbon, and the fate of this carbon remains unknown. Microorganisms will play a central role in its fate, and their viruses could modulate that impact via induced mortality and metabolic controls. Because of the challenges of recovering viruses from soils, little is known about soil viruses or their role(s) in microbial biogeochemical cycling. Here, we describe 53 viral populations (viral operational taxonomic units [vOTUs]) recovered from seven quantitatively derived (i.e., not multiple-displacement-amplified) viral-particle metagenomes (viromes) along a permafrost thaw gradient at the Stordalen Mire field site in northern Sweden. Only 15% of these vOTUs had genetic similarity to publicly available viruses in the RefSeq database, and ∼30% of the genes could be annotated, supporting the concept of soils as reservoirs of substantial undescribed viral genetic diversity. The vOTUs exhibited distinct ecology, with different distributions along the thaw gradient habitats, and a shift from soil-virus-like assemblages in the dry palsas to aquatic-virus-like assemblages in the inundated fen. Seventeen vOTUs were linked to microbial hosts ( in silico ), implicating viruses in infecting abundant microbial lineages from Acidobacteria , Verrucomicrobia , and Deltaproteobacteria , including those encoding key biogeochemical functions such as organic matter degradation. Thirty auxiliary metabolic genes (AMGs) were identified and suggested virus-mediated modulation of central carbon metabolism, soil organic matter degradation, polysaccharide binding, and regulation of sporulation. Together, these findings suggest that these soil viruses have distinct ecology, impact host-mediated biogeochemistry, and likely impact ecosystem function in the rapidly changing Arctic. IMPORTANCE This work is part of a 10-year project to examine thawing permafrost peatlands and is the first virome-particle-based approach to characterize viruses in these systems. This method yielded >2-fold-more viral populations (vOTUs) per gigabase of metagenome than vOTUs derived from bulk-soil metagenomes from the same site (J. B. Emerson, S. Roux, J. R. Brum, B. Bolduc, et al., Nat Microbiol 3:870–880, 2018, https://doi.org/10.1038/s41564-018-0190-y). We compared the ecology of the recovered vOTUs along a permafrost thaw gradient and found (i) habitat specificity, (ii) a shift in viral community identity from soil-like to aquatic-like viruses, (iii) infection of dominant microbial hosts, and (iv) carriage of host metabolic genes. These vOTUs can impact ecosystem carbon processing via top-down (inferred from lysing dominant microbial hosts) and bottom-up (inferred from carriage of auxiliary metabolic genes) controls. This work serves as a foundation which future studies can build upon to increase our understanding of the soil virosphere and how viruses affect soil ecosystem services.},
doi = {10.1128/mSystems.00076-18},
journal = {mSystems},
number = 5,
volume = 3,
place = {United States},
year = {Tue Oct 02 00:00:00 EDT 2018},
month = {Tue Oct 02 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1128/mSystems.00076-18

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Comparative metagenomics of microbial traits within oceanic viral communities
journal, February 2011

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Long-term CO2 production following permafrost thaw
journal, July 2013

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Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses
journal, July 2014

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Functional metagenomic profiling of nine biomes
journal, March 2008

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IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
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The Distribution, Evolution, and Roles of Gene Transfer Agents in Prokaryotic Genetic Exchange
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The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

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Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers
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Streptomyces aureofaciens whiB gene encoding putative transcription factor essential for differentiation
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Thawing sub-arctic permafrost: Effects on vegetation and methane emissions
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Phage-Host Interaction: an Ecological Perspective
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The microbial ecology of permafrost
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Multiple displacement amplification compromises quantitative analysis of metagenomes
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Characterization of Novel Bacteriophages for Biocontrol of Bacterial Blight in Leek Caused by Pseudomonas syringae pv. porri
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Viruses in extreme environments
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Fast gapped-read alignment with Bowtie 2
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Insights into the function of the WhiB-like protein of mycobacteriophage TM4 - a transcriptional inhibitor of WhiB2: WhiBTM4 and WhiB2
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Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory
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Diverse uncultivated ultra-small bacterial cells in groundwater
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Linking environmental prokaryotic viruses and their host through CRISPRs
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Environmental microbiology through the lens of high-throughput DNA sequencing: Synopsis of current platforms and bioinformatics approaches
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Marine Viruses: Truth or Dare
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Pathway of Glucose Catabolism by Strain VeGlc2, an Anaerobe Belonging to the Verrucomicrobiales Lineage of Bacterial Descent
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The bright side of microbial dark matter: lessons learned from the uncultivated majority
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Marine Viruses: Key Players in Marine Ecosystems
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Viral dark matter and virus–host interactions resolved from publicly available microbial genomes
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Identification of four genes involved in the lysogenic pathway of theSalmonella newington bacterial virus ?34
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CsCl Density Gradient Centrifugation Studies of Intact Bacterial Cells
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The Sphagnome Project: enabling ecological and evolutionary insights through a genus-level sequencing project
journal, October 2017

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Laboratory procedures to generate viral metagenomes
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Crass: identification and reconstruction of CRISPR from unassembled metagenomic data
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Network analyses structure genetic diversity in independent genetic worlds
journal, December 2009

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Metagenomic and Small-Subunit rRNA Analyses Reveal the Genetic Diversity of Bacteria, Archaea, Fungi, and Viruses in Soil
journal, September 2007

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Toward an Ecological Classification of soil Bacteria
journal, June 2007

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