Abstract
Permafrost thawing results in the formation of thermokarst lakes, which are biogeochemical hotspots in northern landscapes and strong emitters of greenhouse gasses to the atmosphere. Most studies of thermokarst lakes have been in summer, despite the predominance of winter and ice-cover over much of the year, and the microbial ecology of these waters under ice remains poorly understood. Here we first compared the summer versus winter microbiomes of a subarctic thermokarst lake using DNA- and RNA-based 16S rRNA amplicon sequencing and qPCR. We then applied comparative metagenomics and used genomic bin reconstruction to compare the two seasons for changes in potential metabolic functions in the thermokarst lake microbiome. In summer, the microbial community was dominated by Actinobacteria and Betaproteobacteria, with phototrophic and aerobic pathways consistent with the utilization of labile and photodegraded substrates. The microbial community was strikingly different in winter, with dominance of methanogens, Planctomycetes, Chloroflexi and Deltaproteobacteria, along with various taxa of the Patescibacteria/Candidate Phyla Radiation (Parcubacteria, Microgenomates, Omnitrophica, Aminicenantes). The latter group was underestimated or absent in the amplicon survey, but accounted for about a third of the metagenomic reads. The winter lineages were associated with multiple reductive metabolic processes, fermentations and pathways for the mobilization and degradation of complex organic matter, along with a strong potential for syntrophy or cross-feeding. The results imply that the summer community represents a transient stage of the annual cycle, and that carbon dioxide and methane production continue through the prolonged season of ice cover via a taxonomically distinct winter community and diverse mechanisms of permafrost carbon transformation.
Highlights
Northern landscapes are experiencing rapid change due to climate warming, with large scale thawing and erosion of permafrost soils in many regions (Oliva and Fritz, 2018)
Archaea accounted for only 1% of the total prokaryotes in both the quantitative PCR (qPCR) and metagenomic analyses, but 7% and 17% in winter
Additional phyla, notably Microgenomates, Aminicenantes and Acetothermia, were solely identified by PCR-free metagenomic sequencing. These latter phyla collectively represented a third of the thermokarst lake microbial community in both summer and winter samples, yet were not detected in previous reports based on 16S rRNA gene amplicons (Crevecoeur et al, 2015; Wurzbacher et al, 2017)
Summary
Northern landscapes are experiencing rapid change due to climate warming, with large scale thawing and erosion of permafrost soils in many regions (Oliva and Fritz, 2018). Decomposition and greenhouse gas emission rates from northern soils are variable (Parmentier et al, 2017), and some of the highest CH4 emissions of the permafrost region have been measured in thermokarst lakes and ponds (Matveev et al, 2016). These open waters form by thawing of ice-rich permafrost, which causes surface collapse and the creation of basins that fill with meltwater and precipitation. Calculations suggest that the rapid thaw of sediments beneath thermokarst lakes by the latent heat of the water body could more than double the rate of carbon release from these abundant northern lakes by the end of the century (Walter Anthony et al, 2018)
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