The Role of Viruses in the Carbon Cycle Along a Permafrost Thaw Gradient

Abstract:

Permafrost is thawing due to elevated temperatures that result from climate change. Since permafrost accounts for 30%-50% of global soil carbon (C), it is important to understand how thawing permafrost will impact the release of greenhouse gasses. Microbial communities play a critical role in the terrestrial C cycle, but viruses are less well studied in soils. However, in marine systems, viruses are known to impact C cycling by controlling host microbial communities via predation, transferring genes between hosts, and metabolically reprogramming host cells via regulatory take-over and encoding auxiliary metabolic genes (AMGs). Here, we examined viruses along a permafrost thaw gradient (palsa, bog, and fen) in Stordalen Mire, Sweden over eight years (2010-2017). We used data from bulk metagenomic sequencing and viral eco-genomic analyses in order to assess the extent to which viruses play an ecological role in soils.

In total, we identified 4,168 unique viral populations (≥ 10 kb contigs dereplicated at 95% average nucleotide identity and 80% coverage). Taxonomically, gene-sharing networks organized these viral populations (approximately species-level taxa) into 617 novel genera (compared to NCBI Viral RefSeq). Viral communities appear to separate based on the thaw gradient. However, many viral populations were shared across sites. For example, in the bog, almost 50% of viral populations are shared with at least one other site. To link these viruses to C cycling, we in silico predicted hosts for our viruses, using metagenome-assembled-genomes (MAGs) that were generated from the same samples. We found 26 MAGs that potentially serve as hosts for 42 viruses, using CRISPR spacer matching. Of these MAGs, the majority (77%) are putative key C cyclers, implicating viruses in C cycling via infection. In addition, we identified AMGs in viral sequences that were involved in central C metabolism, including glycolysis, pentose phosphate, and TCA cycle. We also found diverse metabolic genes, including many involved in sulfur, nitrogen, and methane cycles, and carbon degradation (e.g. glycoside hydrolase families). Together, these results suggest that soil viruses may play an ecological role in permafrost via infecting putative key C players and encoding auxiliary metabolic genes associated with C and other nutrient cycles.