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Title: Host-linked soil viral ecology along a permafrost thaw gradient

Abstract

Climate change threatens to release abundant carbon that is sequestered at high latitudes, but the constraints on microbial metabolisms that mediate the release of methane and carbon dioxide are poorly understood. The role of viruses, which are known to affect microbial dynamics, metabolism and biogeochemistry in the oceans, remains largely unexplored in soil. Here, we aimed to investigate how viruses influence microbial ecology and carbon metabolism in peatland soils along a permafrost thaw gradient in Sweden. We recovered 1,907 viral populations (genomes and large genome fragments) from 197 bulk soil and size-fractionated metagenomes, 58% of which were detected in metatranscriptomes and presumed to be active. In silico predictions linked 35% of the viruses to microbial host populations, highlighting likely viral predators of key carbon-cycling microorganisms, including methanogens and methanotrophs. Lineage-specific virus/host ratios varied, suggesting that viral infection dynamics may differentially impact microbial responses to a changing climate. Virus-encoded glycoside hydrolases, including an endomannanase with confirmed functional activity, indicated that viruses influence complex carbon degradation and that viral abundances were significant predictors of methane dynamics. In conclusion, these findings suggest that viruses may impact ecosystem function in climate-critical, terrestrial habitats and identify multiple potential viral contributions to soil carbon cycling.

Authors:
 [1];  [2];  [3];  [4];  [5];  [4];  [5];  [4];  [6];  [5];  [7];  [7];  [4];  [8];  [8]; ORCiD logo [6];  [4];  [9];  [7];  [10] more »;  [5];  [4]; ORCiD logo [4] « less
  1. The Ohio State Univ., Columbus, OH (United States); Univ. of California, Davis, Davis, CA (United States)
  2. The Ohio State Univ., Columbus, OH (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. The Ohio State Univ., Columbus, OH (United States); Louisiana State Univ., Baton Rouge, LA (United States)
  4. The Ohio State Univ., Columbus, OH (United States)
  5. Univ. of Queensland, Brisbane, Queensland (Australia)
  6. Norwegian Univ. of Life Sciences, As (Norway)
  7. Florida State Univ., Tallahassee, FL (United States)
  8. Univ. of New Hampshire, Durham, NH (United States)
  9. Stockholm Univ., Stockholm (Sweden)
  10. Univ. of Arizona, Tucson, AZ (United States)
Publication Date:
Research Org.:
Univ. of Arizona, Tucson, AZ (United States); Ohio State Univ., Columbus, ON (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1486876
Grant/Contract Number:  
SC0004632; SC0010580; SC0016440
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 8; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Emerson, Joanne B., Roux, Simon, Brum, Jennifer R., Bolduc, Benjamin, Woodcroft, Ben J., Jang, Ho Bin, Singleton, Caitlin M., Solden, Lindsey M., Naas, Adrian E., Boyd, Joel A., Hodgkins, Suzanne B., Wilson, Rachel M., Trubl, Gareth, Li, Changsheng, Frolking, Steve, Pope, Phillip B., Wrighton, Kelly C., Crill, Patrick M., Chanton, Jeffrey P., Saleska, Scott R., Tyson, Gene W., Rich, Virginia I., and Sullivan, Matthew B. Host-linked soil viral ecology along a permafrost thaw gradient. United States: N. p., 2018. Web. doi:10.1038/s41564-018-0190-y.
Emerson, Joanne B., Roux, Simon, Brum, Jennifer R., Bolduc, Benjamin, Woodcroft, Ben J., Jang, Ho Bin, Singleton, Caitlin M., Solden, Lindsey M., Naas, Adrian E., Boyd, Joel A., Hodgkins, Suzanne B., Wilson, Rachel M., Trubl, Gareth, Li, Changsheng, Frolking, Steve, Pope, Phillip B., Wrighton, Kelly C., Crill, Patrick M., Chanton, Jeffrey P., Saleska, Scott R., Tyson, Gene W., Rich, Virginia I., & Sullivan, Matthew B. Host-linked soil viral ecology along a permafrost thaw gradient. United States. doi:10.1038/s41564-018-0190-y.
Emerson, Joanne B., Roux, Simon, Brum, Jennifer R., Bolduc, Benjamin, Woodcroft, Ben J., Jang, Ho Bin, Singleton, Caitlin M., Solden, Lindsey M., Naas, Adrian E., Boyd, Joel A., Hodgkins, Suzanne B., Wilson, Rachel M., Trubl, Gareth, Li, Changsheng, Frolking, Steve, Pope, Phillip B., Wrighton, Kelly C., Crill, Patrick M., Chanton, Jeffrey P., Saleska, Scott R., Tyson, Gene W., Rich, Virginia I., and Sullivan, Matthew B. Mon . "Host-linked soil viral ecology along a permafrost thaw gradient". United States. doi:10.1038/s41564-018-0190-y. https://www.osti.gov/servlets/purl/1486876.
@article{osti_1486876,
title = {Host-linked soil viral ecology along a permafrost thaw gradient},
author = {Emerson, Joanne B. and Roux, Simon and Brum, Jennifer R. and Bolduc, Benjamin and Woodcroft, Ben J. and Jang, Ho Bin and Singleton, Caitlin M. and Solden, Lindsey M. and Naas, Adrian E. and Boyd, Joel A. and Hodgkins, Suzanne B. and Wilson, Rachel M. and Trubl, Gareth and Li, Changsheng and Frolking, Steve and Pope, Phillip B. and Wrighton, Kelly C. and Crill, Patrick M. and Chanton, Jeffrey P. and Saleska, Scott R. and Tyson, Gene W. and Rich, Virginia I. and Sullivan, Matthew B.},
abstractNote = {Climate change threatens to release abundant carbon that is sequestered at high latitudes, but the constraints on microbial metabolisms that mediate the release of methane and carbon dioxide are poorly understood. The role of viruses, which are known to affect microbial dynamics, metabolism and biogeochemistry in the oceans, remains largely unexplored in soil. Here, we aimed to investigate how viruses influence microbial ecology and carbon metabolism in peatland soils along a permafrost thaw gradient in Sweden. We recovered 1,907 viral populations (genomes and large genome fragments) from 197 bulk soil and size-fractionated metagenomes, 58% of which were detected in metatranscriptomes and presumed to be active. In silico predictions linked 35% of the viruses to microbial host populations, highlighting likely viral predators of key carbon-cycling microorganisms, including methanogens and methanotrophs. Lineage-specific virus/host ratios varied, suggesting that viral infection dynamics may differentially impact microbial responses to a changing climate. Virus-encoded glycoside hydrolases, including an endomannanase with confirmed functional activity, indicated that viruses influence complex carbon degradation and that viral abundances were significant predictors of methane dynamics. In conclusion, these findings suggest that viruses may impact ecosystem function in climate-critical, terrestrial habitats and identify multiple potential viral contributions to soil carbon cycling.},
doi = {10.1038/s41564-018-0190-y},
journal = {Nature Microbiology},
number = 8,
volume = 3,
place = {United States},
year = {2018},
month = {7}
}

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Cited by: 24 works
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Figures / Tables:

Fig. 1 Fig. 1: Overview of Stordalen Mire soil viruses. a, An accumulation curve of viral populations in bulk soil metagenomes (n = 201). The means are represented by red circles and 200 randomizations of sample order are shown in teal. b, A network of shared predicted protein content among Stordalen Miremore » viruses (n = 1,907), RefSeq prokaryotic viral genomes (n = 2,010) and soil-associated viral contigs > 10 kb from Paez-Espino et al. (n = 3,112) and Roux et al. (n = 2,040). Nodes (circles) represent genomes and contigs, and the shared edges (lines) indicate shared protein content. c, Pie charts indicate per cent relative abundances of Stordalen Mire viral populations (n = 828, 782 and 475 populations detected in palsa, bog and fen, respectively; palsa: n = 72 samples, bog: n = 65 samples and fen: n = 64 samples) that: have predicted taxonomy (green), have unknown taxonomy but share a viral cluster (VC) with viruses from public datasets (from b, blue), or were previously unknown (in a Stordalen Mire-exclusive VC, yellow). The bar graphs indicate the per cent relative abundances of viral taxa in each habitat, considering only viruses with predicted taxonomy (n = 323). d, Principal coordinates analysis (PCoA) of viral community composition, as derived from read mapping to viral contigs (n = 1,907) and Bray–Curtis dissimilarities; each point is one sample (n = 201). The analysis of similarity (ANOSIM) statistics consider viral community composition grouped by habitat (palsa: n = 72 samples, bog: n = 65 samples and fen: n = 64 samples).« less

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