Metatranscriptomics reveals declines in ice cover influence winter viral community activity

Freshwater lakes are sentinels of environmental change, and climate change-driven declines in ice cover have been shown to disrupt aquatic communities and jeopardize ecosystem services. Viruses shape microbial communities and regulate biogeochemical cycles by acting as top-down controls, yet there is relatively little known about how declining ice cover will influence viral community activity. Lake Erie is a critical freshwater ecosystem and serves as a model system to assess how ice cover extent will affect winter limnology. We surveyed size selected surface water metatranscriptomes for conserved viral hallmark genes as a proxy for active virus populations and compared activity profiles between ice-covered and ice-free conditions from two contrasting winters. Active virus communities were present in both conditions, spanning diverse phylogenetic clades of bacteriophage (Caudovirales), giant viruses (Nucleocytoviricota), and RNA viruses (Orthornavirae). However, viral activity was significantly shaped by the extent of ice cover. Notably, viral richness and relative transcript abundance in the surface waters were reduced under ice relative to the ice-free conditions. Correlations with microbial community metrics suggest the differences in viral communities are at least in part driven by the decreased winter diatom bloom associated with declines in ice cover. Overall, our data suggest viral community activity is influenced by ice cover extent, and viruses may serve as sentinels of environmental disturbance and ecosystem response(s) to climate change. IMPORTANCEAs ice cover is projected to become increasingly rare on large temperate lakes, there is a need to understand how microbial communities during winter months might respond to these changing ice-cover conditions. Despite the documented controls viruses have on microbial communities, little is known regarding the relationship between virus activity and ice cover extent. By using metatranscriptomics to investigate virus communities, we show that viral community activity is sensitive to ice cover extent, likely due in part to ice cover-driven shifts in host community structure. This work serves to build our understanding of how viral communities will function in a future, potentially ice-free, climate.