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 reco...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2018-10-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00076-18 |
| _version_ | 1818733840902914048 |
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| author | Gareth Trubl Ho Bin Jang Simon Roux Joanne B. Emerson Natalie Solonenko Dean R. Vik Lindsey Solden Jared Ellenbogen Alexander T. Runyon Benjamin Bolduc Ben J. Woodcroft Scott R. Saleska Gene W. Tyson Kelly C. Wrighton Matthew B. Sullivan Virginia I. Rich |
| author_facet | Gareth Trubl Ho Bin Jang Simon Roux Joanne B. Emerson Natalie Solonenko Dean R. Vik Lindsey Solden Jared Ellenbogen Alexander T. Runyon Benjamin Bolduc Ben J. Woodcroft Scott R. Saleska Gene W. Tyson Kelly C. Wrighton Matthew B. Sullivan Virginia I. Rich |
| author_sort | Gareth Trubl |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-17T23:55:52Z |
| format | Article |
| id | doaj.art-c96d6a9b162d4928ab463475ebcb7118 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-17T23:55:52Z |
| publishDate | 2018-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-c96d6a9b162d4928ab463475ebcb71182022-12-21T21:28:04ZengAmerican Society for MicrobiologymSystems2379-50772018-10-013510.1128/mSystems.00076-18Soil Viruses Are Underexplored Players in Ecosystem Carbon ProcessingGareth Trubl0Ho Bin Jang1Simon Roux2Joanne B. Emerson3Natalie Solonenko4Dean R. Vik5Lindsey Solden6Jared Ellenbogen7Alexander T. Runyon8Benjamin Bolduc9Ben J. Woodcroft10Scott R. Saleska11Gene W. Tyson12Kelly C. Wrighton13Matthew B. Sullivan14Virginia I. Rich15Department of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USAAustralian Centre for Ecogenomics, The University of Queensland, St. Lucia, Queensland, AustraliaDepartment of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, USAAustralian Centre for Ecogenomics, The University of Queensland, St. Lucia, Queensland, AustraliaDepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USADepartment of Microbiology, The Ohio State University, Columbus, Ohio, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mSystems.00076-18Arcticcarbon cyclingenvironmental microbiologymicrobial ecologypeatlandspermafrost |
| spellingShingle | Gareth Trubl Ho Bin Jang Simon Roux Joanne B. Emerson Natalie Solonenko Dean R. Vik Lindsey Solden Jared Ellenbogen Alexander T. Runyon Benjamin Bolduc Ben J. Woodcroft Scott R. Saleska Gene W. Tyson Kelly C. Wrighton Matthew B. Sullivan Virginia I. Rich Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing mSystems Arctic carbon cycling environmental microbiology microbial ecology peatlands permafrost |
| title | 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_short | Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing |
| title_sort | soil viruses are underexplored players in ecosystem carbon processing |
| topic | Arctic carbon cycling environmental microbiology microbial ecology peatlands permafrost |
| url | https://journals.asm.org/doi/10.1128/mSystems.00076-18 |
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