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Title: Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing

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:
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Publication Date:
Grant/Contract Number:
SC0004632; SC0010580; SC0016440
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
Sponsoring Org:
USDOE
Country of Publication:
United States
Language:
English
OSTI Identifier:
1475081

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., 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. 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., and Bordenstein, ed., Seth. 2018. "Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing". United States. doi: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 = {2018},
month = {10}
}

Works referenced in this record:

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000
  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Search and clustering orders of magnitude faster than BLAST
journal, August 2010