Soil viruses are underexplored players in ecosystem carbon processing
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 vi...
Published in: | mSystems |
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Main Authors: | , , , , , , , , , , , , , , , |
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Format: | Article in Journal/Newspaper |
Language: | English |
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American Society for Microbiology
2018
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Online Access: | https://espace.library.uq.edu.au/view/UQ:46ea04e |
id |
ftunivqespace:oai:espace.library.uq.edu.au:UQ:46ea04e |
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record_format |
openpolar |
institution |
Open Polar |
collection |
The University of Queensland: UQ eSpace |
op_collection_id |
ftunivqespace |
language |
English |
topic |
Arctic Carbon cycling Environmental microbiology Microbial ecology Peatlands Permafrost Soil microbiology Soil viromics Viral ecology Viromes 1105 Ecology Evolution Behavior and Systematics 1303 Biochemistry 1311 Genetics 1312 Molecular Biology 1314 Physiology 1706 Computer Science Applications 2404 Microbiology 2611 Modelling and Simulation |
spellingShingle |
Arctic Carbon cycling Environmental microbiology Microbial ecology Peatlands Permafrost Soil microbiology Soil viromics Viral ecology Viromes 1105 Ecology Evolution Behavior and Systematics 1303 Biochemistry 1311 Genetics 1312 Molecular Biology 1314 Physiology 1706 Computer Science Applications 2404 Microbiology 2611 Modelling and Simulation 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. Soil viruses are underexplored players in ecosystem carbon processing |
topic_facet |
Arctic Carbon cycling Environmental microbiology Microbial ecology Peatlands Permafrost Soil microbiology Soil viromics Viral ecology Viromes 1105 Ecology Evolution Behavior and Systematics 1303 Biochemistry 1311 Genetics 1312 Molecular Biology 1314 Physiology 1706 Computer Science Applications 2404 Microbiology 2611 Modelling and Simulation |
description |
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. |
author2 |
Bordenstein, Seth |
format |
Article in Journal/Newspaper |
author |
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. |
author_facet |
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. |
author_sort |
Trubl, Gareth |
title |
Soil viruses are underexplored players in ecosystem carbon processing |
title_short |
Soil viruses are underexplored players in ecosystem carbon processing |
title_full |
Soil viruses are underexplored players in ecosystem carbon processing |
title_fullStr |
Soil viruses are underexplored players in ecosystem carbon processing |
title_full_unstemmed |
Soil viruses are underexplored players in ecosystem carbon processing |
title_sort |
soil viruses are underexplored players in ecosystem carbon processing |
publisher |
American Society for Microbiology |
publishDate |
2018 |
url |
https://espace.library.uq.edu.au/view/UQ:46ea04e |
long_lat |
ENVELOPE(168.733,168.733,-71.583,-71.583) ENVELOPE(7.337,7.337,62.510,62.510) |
geographic |
Arctic Emerson Stordalen |
geographic_facet |
Arctic Emerson Stordalen |
genre |
Arctic Northern Sweden palsas permafrost |
genre_facet |
Arctic Northern Sweden palsas permafrost |
op_relation |
doi:10.1128/mSystems.00076-18 issn:2379-5077 orcid:0000-0003-0670-7480 orcid:0000-0001-8559-9427 Not set DBI-0735191 DBI-1265383 DE-SC0004632 DE-SC0010580 DE-SC0016440 3790 |
op_doi |
https://doi.org/10.1128/mSystems.00076-18 |
container_title |
mSystems |
container_volume |
3 |
container_issue |
5 |
_version_ |
1766339451868413952 |
spelling |
ftunivqespace:oai:espace.library.uq.edu.au:UQ:46ea04e 2023-05-15T15:08:01+02:00 Soil viruses are underexplored players in ecosystem carbon processing 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, Seth 2018-09-01 https://espace.library.uq.edu.au/view/UQ:46ea04e eng eng American Society for Microbiology doi:10.1128/mSystems.00076-18 issn:2379-5077 orcid:0000-0003-0670-7480 orcid:0000-0001-8559-9427 Not set DBI-0735191 DBI-1265383 DE-SC0004632 DE-SC0010580 DE-SC0016440 3790 Arctic Carbon cycling Environmental microbiology Microbial ecology Peatlands Permafrost Soil microbiology Soil viromics Viral ecology Viromes 1105 Ecology Evolution Behavior and Systematics 1303 Biochemistry 1311 Genetics 1312 Molecular Biology 1314 Physiology 1706 Computer Science Applications 2404 Microbiology 2611 Modelling and Simulation Journal Article 2018 ftunivqespace https://doi.org/10.1128/mSystems.00076-18 2020-12-29T00:53:42Z 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. Article in Journal/Newspaper Arctic Northern Sweden palsas permafrost The University of Queensland: UQ eSpace Arctic Emerson ENVELOPE(168.733,168.733,-71.583,-71.583) Stordalen ENVELOPE(7.337,7.337,62.510,62.510) mSystems 3 5 |