Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations

Abstract Background Peatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions. Despite mounting evidence for viral contributions to these processes in peatlands underlain with permafr...

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Autores principales: Anneliek M. ter Horst, Christian Santos-Medellín, Jackson W. Sorensen, Laura A. Zinke, Rachel M. Wilson, Eric R. Johnston, Gareth G. Trubl, Jennifer Pett-Ridge, Steven J. Blazewicz, Paul J. Hanson, Jeffrey P. Chanton, Christopher W. Schadt, Joel E. Kostka, Joanne B. Emerson
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spelling oai:doaj.org-article:8af0bdecc6b14bce80b36a0afe40c38a2021-11-28T12:08:13ZMinnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations10.1186/s40168-021-01156-02049-2618https://doaj.org/article/8af0bdecc6b14bce80b36a0afe40c38a2021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01156-0https://doaj.org/toc/2049-2618Abstract Background Peatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions. Despite mounting evidence for viral contributions to these processes in peatlands underlain with permafrost, little is known about viruses in other peatlands. More generally, soil viral biogeography and its potential drivers are poorly understood at both local and global scales. Here, 87 metagenomes and five viral size-fraction metagenomes (viromes) from a boreal peatland in northern Minnesota (the SPRUCE whole-ecosystem warming experiment and surrounding bog) were analyzed for dsDNA viral community ecological patterns, and the recovered viral populations (vOTUs) were compared with our curated PIGEON database of 266,125 vOTUs from diverse ecosystems. Results Within the SPRUCE experiment, viral community composition was significantly correlated with peat depth, water content, and carbon chemistry, including CH4 and CO2 concentrations, but not with temperature during the first 2 years of warming treatments. Peat vOTUs with aquatic-like signatures (shared predicted protein content with marine and/or freshwater vOTUs) were significantly enriched in more waterlogged surface peat depths. Predicted host ranges for SPRUCE vOTUs were relatively narrow, generally within a single bacterial genus. Of the 4326 SPRUCE vOTUs, 164 were previously detected in other soils, mostly peatlands. None of the previously identified 202,371 marine and freshwater vOTUs in our PIGEON database were detected in SPRUCE peat, but 0.4% of 80,714 viral clusters (VCs, grouped by predicted protein content) were shared between soil and aquatic environments. On a per-sample basis, vOTU recovery was 32 times higher from viromes compared with total metagenomes. Conclusions Results suggest strong viral “species” boundaries between terrestrial and aquatic ecosystems and to some extent between peat and other soils, with differences less pronounced at higher taxonomic levels. The significant enrichment of aquatic-like vOTUs in more waterlogged peat suggests that viruses may also exhibit niche partitioning on more local scales. These patterns are presumably driven in part by host ecology, consistent with the predicted narrow host ranges. Although more samples and increased sequencing depth improved vOTU recovery from total metagenomes, the substantially higher per-sample vOTU recovery after viral particle enrichment highlights the utility of soil viromics. Video abstract The importance of Minnesota peat viromes in revealing terrestrial and aquatic niche partitioning for viral populationsAnneliek M. ter HorstChristian Santos-MedellínJackson W. SorensenLaura A. ZinkeRachel M. WilsonEric R. JohnstonGareth G. TrublJennifer Pett-RidgeSteven J. BlazewiczPaul J. HansonJeffrey P. ChantonChristopher W. SchadtJoel E. KostkaJoanne B. EmersonBMCarticleViral ecologyViromicsSoil virusesSoil microbial ecologyPeatMetagenomicsMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-18 (2021)
institution DOAJ
collection DOAJ
language EN
topic Viral ecology
Viromics
Soil viruses
Soil microbial ecology
Peat
Metagenomics
Microbial ecology
QR100-130
spellingShingle Viral ecology
Viromics
Soil viruses
Soil microbial ecology
Peat
Metagenomics
Microbial ecology
QR100-130
Anneliek M. ter Horst
Christian Santos-Medellín
Jackson W. Sorensen
Laura A. Zinke
Rachel M. Wilson
Eric R. Johnston
Gareth G. Trubl
Jennifer Pett-Ridge
Steven J. Blazewicz
Paul J. Hanson
Jeffrey P. Chanton
Christopher W. Schadt
Joel E. Kostka
Joanne B. Emerson
Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
description Abstract Background Peatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions. Despite mounting evidence for viral contributions to these processes in peatlands underlain with permafrost, little is known about viruses in other peatlands. More generally, soil viral biogeography and its potential drivers are poorly understood at both local and global scales. Here, 87 metagenomes and five viral size-fraction metagenomes (viromes) from a boreal peatland in northern Minnesota (the SPRUCE whole-ecosystem warming experiment and surrounding bog) were analyzed for dsDNA viral community ecological patterns, and the recovered viral populations (vOTUs) were compared with our curated PIGEON database of 266,125 vOTUs from diverse ecosystems. Results Within the SPRUCE experiment, viral community composition was significantly correlated with peat depth, water content, and carbon chemistry, including CH4 and CO2 concentrations, but not with temperature during the first 2 years of warming treatments. Peat vOTUs with aquatic-like signatures (shared predicted protein content with marine and/or freshwater vOTUs) were significantly enriched in more waterlogged surface peat depths. Predicted host ranges for SPRUCE vOTUs were relatively narrow, generally within a single bacterial genus. Of the 4326 SPRUCE vOTUs, 164 were previously detected in other soils, mostly peatlands. None of the previously identified 202,371 marine and freshwater vOTUs in our PIGEON database were detected in SPRUCE peat, but 0.4% of 80,714 viral clusters (VCs, grouped by predicted protein content) were shared between soil and aquatic environments. On a per-sample basis, vOTU recovery was 32 times higher from viromes compared with total metagenomes. Conclusions Results suggest strong viral “species” boundaries between terrestrial and aquatic ecosystems and to some extent between peat and other soils, with differences less pronounced at higher taxonomic levels. The significant enrichment of aquatic-like vOTUs in more waterlogged peat suggests that viruses may also exhibit niche partitioning on more local scales. These patterns are presumably driven in part by host ecology, consistent with the predicted narrow host ranges. Although more samples and increased sequencing depth improved vOTU recovery from total metagenomes, the substantially higher per-sample vOTU recovery after viral particle enrichment highlights the utility of soil viromics. Video abstract The importance of Minnesota peat viromes in revealing terrestrial and aquatic niche partitioning for viral populations
format article
author Anneliek M. ter Horst
Christian Santos-Medellín
Jackson W. Sorensen
Laura A. Zinke
Rachel M. Wilson
Eric R. Johnston
Gareth G. Trubl
Jennifer Pett-Ridge
Steven J. Blazewicz
Paul J. Hanson
Jeffrey P. Chanton
Christopher W. Schadt
Joel E. Kostka
Joanne B. Emerson
author_facet Anneliek M. ter Horst
Christian Santos-Medellín
Jackson W. Sorensen
Laura A. Zinke
Rachel M. Wilson
Eric R. Johnston
Gareth G. Trubl
Jennifer Pett-Ridge
Steven J. Blazewicz
Paul J. Hanson
Jeffrey P. Chanton
Christopher W. Schadt
Joel E. Kostka
Joanne B. Emerson
author_sort Anneliek M. ter Horst
title Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
title_short Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
title_full Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
title_fullStr Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
title_full_unstemmed Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
title_sort minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations
publisher BMC
publishDate 2021
url https://doaj.org/article/8af0bdecc6b14bce80b36a0afe40c38a
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