Active virus-host interactions at sub-freezing temperatures in Arctic peat soil

Abstract

Background Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake and is primarily driven by microbial decomposers. Viruses modulate microbial carbon cycling via induced mortality and metabolic controls, but it is unknown whether viruses are active under winter conditions (anoxic and sub-freezing temperatures). Results We used stable isotope probing (SIP) targeted metagenomics to reveal the genomic potential of active soil microbial populations under simulated winter conditions, with an emphasis on viruses and virus-host dynamics. Arctic peat soils from the Bonanza Creek Long-Term Ecological Research site in Alaska were incubated under sub-freezing anoxic conditions with H218O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO2) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up 18O in soil and respired CO2 throughout the incubation. Active bacterial populations represented only a small portion of the detected microbial community and were capable of fermentation and organic matter degradation. In contrast, active viral populations represented a large portion of the detected viral community and one third were linked to active bacterial populations. We identified 86 auxiliary metabolic genes and other environmentally relevant genes. The majority of these genes were carried by active viral populations and had diverse functions such as carbon utilization and scavenging that could provide their host with a fitness advantage for utilizing much-needed carbon sources or acquiring essential nutrients. Conclusions Overall, there was a stark difference in the identity and function of the active bacterial and viral community compared to the unlabeled community that would have been overlooked with a non-targeted standard metagenomic analysis. Our results illustrate that substantial active virus-host interactions occur in sub-freezing anoxic conditions and highlight viruses as a major community-structuring agent that likely modulates carbon loss in peat soils during winter, which may be pivotal for understanding the future fate of arctic soils' vast carbon stocks.

Spatial turnover of soil viral populations and genotypes overlain by cohesive responses to moisture in grasslands

“…Soil microorganisms play key roles in these biogeochemical processes 9,10 , and, by infecting soil microbiota 11 , viruses likely have substantial direct and indirect impacts on the resulting carbon dynamics 12 . More generally, the potential importance of viruses in soils 1,2,13,14 , together with their measured high abundance (10 7 to 10 10 virus-like particles per gram of soil 1 ) and improvements in our ability to sequence and track soil viral genomes 12,15 , has led to a renewed flurry of investigations into soil viral diversity and ecology [3][4][5][16][17][18][19][20][21] . Yet, despite a new appreciation for the vast diversity of soil viruses [3][4][5][16][17][18] , little is known about the factors that govern soil viral community assembly.…”

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Although soil viral abundance, diversity, and potential roles in microbial community dynamics and biogeochemical cycling are beginning to be appreciated [1][2][3][4][5] , little is known about the patterns and drivers of soil viral community composition that underlie their contributions to terrestrial ecology. Here, we analyzed 43 soil viromes from a precipitation manipulation experiment in a Mediterranean grassland in California, USA.

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Substantial differences in soil viral community composition within and among four Northern California habitats

“…3 Soil viral abundance measurements vary substantially, ranging from nearly zero in dry deserts to over 10 9 virus-like particles per gram in wetlands [3]. In the better studied oceans, viruses kill approximately 20% of microbial biomass daily, impacting nutrient and energy cycles [4], and recent work suggests that viruses may be similarly important in terrestrial ecosystems [3,[5][6][7][8][9][10][11][12].…”

“…For example, viruses have been suggested to affect carbon cycling in thawing permafrost peatlands by preying on methanogens and methanotrophs and by encoding glycoside hydrolases to break down complex carbon into simple sugars [2]. Soil viral activity has been demonstrated [2,5,13], and soil viral communities can be spatially structured [14][15][16]. Despite these emerging ecological patterns, comparisons of soil viral diversity within and across habitats are limited.…”

Structural characterization of a soil viral auxiliary metabolic gene encoding a functional chitosanase

“…One of these, a viral gene encoding a glycosyl hydrolase group 5 (GH5) enzyme, was cloned, expressed and found to represent a functional endomannanase 3 . The vast majority of predicted soil viral AMGs have been assigned potential functions solely based on their sequence similarities to annotated genes in microbial genomic databases 1,6 . This approach is however limited in its ability to determine if the AMG is actually expressed and if the protein is functional.…”