Host-linked soil viral ecology along a permafrost thaw gradient

Joanne B. Emerson, Simon Roux, Jennifer R. Brum, Benjamin Bolduc, Ben J. Woodcroft, Ho Bin Jang, Caitlin M. Singleton, Lindsey M. Solden, Adrian E. Naas, Joel A. Boyd, Suzanne B. Hodgkins, Rachel M. Wilson, Gareth Trubl, Changsheng Li, Steve Frolking, Phillip B. Pope, Kelly C. Wrighton, Patrick M. Crill, Jeffrey P. Chanton, Scott R. SaleskaGene W. Tyson, Virginia I. Rich, Matthew B. Sullivan*

*Corresponding author for this work

Research output: Contribution to journalLetterpeer-review

333 Citations (Scopus)

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 1–7 . The role of viruses, which are known to affect microbial dynamics, metabolism and biogeochemistry in the oceans 8–10 , 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. These findings suggest that viruses may impact ecosystem function in climate-critical, terrestrial habitats and identify multiple potential viral contributions to soil carbon cycling.

Original languageEnglish
JournalNature Microbiology
Volume3
Issue number8
Pages (from-to)870-880
Number of pages11
ISSN2058-5276
DOIs
Publication statusPublished - 1 Aug 2018
Externally publishedYes

Bibliographical note

Funding Information:
This research was supported by the US Department of Energy, Office of Science, Office of Biological and Environmental Research, under the Genomic Science program (Awards DE-SC0004632, DE-SC0010580 and DE-SC0016440), with partial support from the Gordon and Betty Moore Foundation (GBMF no. 3305 and 3790) and the US National Science Foundation (OCE no. 1536989) awards to M.B.S., along with high-performance computing resources from the Ohio Supercomputer Center. A.E.N. and P.B.P. were supported by the European Research Council through grant 336355. We thank the IsoGenie 1 and 2 Project Teams and the 2010–2012 field teams for sample collection, particularly C. McCalley and T. Logan, as well as the Abisko Scientific Research Station for sampling infrastructure and support. We thank M. Palace ([email protected]) for generating and allowing us to use the unmanned aerial vehicle image in Supplementary Fig. 1.

Publisher Copyright:
© 2018, The Author(s).

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