Adaptations of DNA viruses are influenced by host and environment with proliferations constrained by environmental niche

Abstract

Viruses are ubiquitous albeit individually constrained by host-range. Less well understood are environmental limitations on virus proliferation. To investigate estuarine viral diversity, niche constraints, and genomic traits of environmental adaptation, we analysed metagenomic and metatranscriptomic data from across an estuarine salinity gradient, including water and sediment habitats. We then expanded our analysis to globally distributed viral genomes. Viral distributions varied by estuary habitat, reflecting prokaryote community patterns, and highlighting that virus-host interactions are strongly influenced by environment. Viral lineages, up until approximately the rank of genus, were largely partitioned by ecological niche based on factors such as salinity and the aquatic-terrestrial divide. Across habitat boundaries, we identified variations in genomic GC content, and genomic signatures of salinity adaptation, particularly in virus major tail and capsid proteins. These included elevated ratios of acidic to basic amino acids and decreased protein isoelectric points at higher salinities which did not solely reflect biases inherited due to reliance on host machinery. Salinity is a well-described physiological stressor for prokaryotes. Results suggest that viruses employ some of the same osmoadaptive strategies independent of adaptation based on host machinery. Our findings indicate that, in addition to host range limitations, successful proliferation of viruses into distinct biomes (e.g. freshwater, saline, terrestrial) is constrained by adaptation to specific ecological niches.