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

Gareth Trubl,Steven J Blazewicz,Jose Liquet-Gonzalez,Janet K Jansson,Jeffrey A Kimbrel,Jennifer Pett-Ridge,Erin E Nuccio,Mark P Waldrop,Peter K Weber

doi:10.1186/s40168-021-01154-2

Abstract

BackgroundWinter 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).ResultsWe 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.ConclusionsOverall, 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.7CT7oo5s6pZcfh9yAbPeefVideo abstract

Highlights

Northern peatlands are important terrestrial ecosystems for carbon (C) storage, estimated to contain one-third of soil C (~1000 gigatons) [1], yet the fate of this C is unknown as these soils are experiencing dramatic changes from anthropogenic climate change [2,3,4]
With the AMGcentric pipeline DRAM-v, we predicted 86 putative Auxiliary metabolic gene (AMG) and other environmentally relevant genes distilled into five functional categories (C utilization, energy, organic nitrogen, transporters, and miscellaneous) from 31 Viral Operational Taxonomic Unit (vOTU) (Table S6); 21 of the vOTUs were active and carried 63 AMGs and other environmentally relevant genes (Fig. 2)
All 145 of the vOTUs we identified as host-linked may be classified as dsDNA bacteriophages

Summary

Introduction

Northern peatlands are important terrestrial ecosystems for carbon (C) storage, estimated to contain one-third of soil C (~1000 gigatons) [1], yet the fate of this C is unknown as these soils are experiencing dramatic changes from anthropogenic climate change [2,3,4]. Recent estimates show substantial winter C loss [9], which may be greater than the average growing season C uptake [10]. While the winter months include large air temperature fluctuations and extreme temperature minimums [11], the temperatures found in much of the soil profile of permafrost or seasonally frozen bogs can remain stable and just below the freezing point (−1 to −5°C) [5, 12, 13]. 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)

Methods

Results

Discussion

Conclusion