Capturing in situ Virus-Host Range and Interaction Dynamics through Gene Fusion with epicPCR

Abstract

Viruses impact microbial diversity, phenotype, and gene flow through virus-host interactions that in turn alter ecology and biogeochemistry. Though metagenomics surveys are rapidly cataloging viral diversity, capturing specific virus-host interactions in situ would identify hosts for novel viruses and reveal influential ecological or environmental factors. We leveraged metagenomics and a high-throughput, cultivation-independent gene fusion technique (epicPCR) to investigate viral diversity and virus-host interactions over time in a critical estuarine environment, the Chesapeake Bay. EpicPCR captured in situ virus-host interactions for viral clades with no closely related database representatives. Abundant freshwater Actinobacteria lineages were the most common hosts for these poorly characterized viruses, and observed viral interactions with one abundant Actinobacterial population (Rhodoluna) were correlated with environmental factors. Tracking virus-host interaction dynamics also revealed ecological differences between multi-host (generalist) and single-host (specialist) viruses. Generalist viruses had significantly longer periods with observed virus-host interactions but specialist viruses were observed interacting with hosts at lower minimum abundances, suggesting more efficient interactions. Together, these observations reveal ecological differences between generalist and specialist viruses that provide insight into evolutionary trade-offs. Capturing in situ interactions with epicPCR revealed environmental and ecological factors that shape virus-host interactions, highlighting epicPCR as a scalable new tool in viral ecology.