Viruses help rewire carbon metabolism in a methane-suppressed peat microcosm

Arctic permafrosts are rapidly thawing in response to climate change, stimulating microbial activity and release of additional greenhouse gases, such as methane. Recently, catechin amendment of thawed permafrost soil microcosms demonstrated >80% decrease in methane production over 35 days compared to unamended controls, with metagenome, metatranscriptome and metabolome analyses revealing a shift in prokaryotic carbon metabolism from a syntrophic network feeding methanogens to one dominated by catechin fermentation. Here we leverage these same data to investigate potential virus impacts on this microbial community metabolism shift. In total, 900 DNA virus operational taxonomic units (vOTUs) were identified as actively lytic based on transcribed structural and lysis genes. Of these, 41% were predicted to infect at least one of 56 transcriptionally active prokaryote genera representing 13 phyla. The most active vOTUs were predicted to infect key catechin-degrading genera including Clostridium and undescribed Bacillota genus JAGFXR01. Temporally, viral communities responded later than prokaryotes to catechin amendment, reflecting a virus production lag to targeting key microbial responders. A single induced vOTU predicted to infect JAGFXR01 dominated the catechin-amended viral community response, with relative abundances 20-156 times higher than its host suggesting intense viral lysis that could release degraded catechin intermediates. Indeed, examination of catechin intermediate gene expression in non-catechin-degraders revealed that they were elevated in catechin-amended samples, suggesting JAGFXR01 lysis products were taken up by non-catechin-degraders as part of community carbon metabolism rewiring. Together, these results place viruses at the heart of carbon rewiring that modulates ecosystem outputs of climate-critical thawing permafrosts.