Abstract
BackgroundPeatlands 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.ResultsWithin 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.ConclusionsResults 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.3EUUqCyiCvMAAvxFuvvQVmVideo abstract The importance of Minnesota peat viromes in revealing terrestrial and aquatic niche partitioning for viral populations
Highlights
Peatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions
The significant enrichment of aquatic-like viral community and population (vOTU) in more waterlogged peat suggests that viruses may exhibit niche partitioning on more local scales
Dataset overview and peat viral population recovery To improve our understanding of peat viral diversity, we leveraged 82 peat metagenomes from cores collected from the Spruce and Peatland Responses Under Changing Environments (SPRUCE) experiment in northern Minnesota, USA in 2015 and 2016, along with five paired viromes and metagenomes that we collected along a transect outside the experimental plots from the same bog in 2018 at near-surface depths
Summary
Peatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions. Viruses are estimated to lyse 20–40% of ocean microbial cells daily, impacting global ocean food webs and the marine C cycle [16,17,18], and viral contributions to terrestrial ecosystems are presumed to be important but are less well understood [6, 13, 14, 19,20,21]. Metatranscriptomic data mining has recently been used to explore RNA viral communities, revealing differences in bulk, rhizosphere, and detritusphere (plant litter-influenced) soil compartments [32], along with potential viral contributions to the ecology of the Sphagnum moss microbiome [33]. We have an array of laboratory and bioinformatics methods for soil viral ecology [7, 15, 23, 31, 34, 36,37,38,39,40,41], we lack a thorough comparative understanding of these approaches and best practices
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