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.
Winter soil processes are critical to the carbon balance of northern ecosystems, yet the microbial ecology governing biogeochemical cycling in frozen soils is largely unknown. We used stable isotope probing targeted metagenomics to reveal the genomic potential of active microbial populations, with an emphasis on viruses, in soils. Peat soils were incubated under simulated winter conditions (subzero and anoxic) with H218O or natural abundance water for 184 and 370 days. Isotope incorporation revealed 46 active bacterial populations (MAGs; spanning 9 bacterial phyla) and 243 active viral populations (vOTUs). Active hosts were predicted for 33% of the active vOTUs and were some of the most abundant MAGs, having capacity for fermentation and carbohydrate utilization. Additionally, almost one-third of vOTUs carried auxiliary metabolic genes spanning five functional categories, highlighting the potential impact of viruses in microbial biogeochemistry. CO2 production throughout the incubation supports our evidence of microbial activities under winter conditions. Our results revealed a multi-trophic and changing microbial community in tandem with a changing viral community targeting dominant active bacteria consistent with the “kill-the-winner” hypothesis. These data have important implications for low-temperature soil processes in northern peatlands and reveal active host-linked soil viral ecology, with potential multifaceted biogeochemical impacts.
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