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Metatranscriptomics has emerged as a tool in microbial ecology that can resolve the functional landscape of both prokaryotes and eukaryotes within a community. In this study, we extend the potential of metatranscriptomics to probe active virus infections and virus-host relationships in marine systems. Polyadenylation-selected RNA-seq data were examined from microbial communities in two productive marine environments: a brown tide bloom event dominated by Aureococcus anophagefferens in Quantuck Bay, NY, and a diatom-dominated plankton community in Narragansett Bay, RI. Active infections by diverse giant viruses (NCLDVs) of algal and non-algal hosts were found at both sites. Ongoing infections of A. anophagefferens by a known Mimiviridae (AaV) were observed during both the peak and decline of the bloom. Bloom decline was also accompanied by increased activity for viruses other than AaV, including (+) ssRNA viruses. In Narragansett Bay, increased temporal reso’lution revealed active NCLDVs with both ‘boom-and-bust’ as well as ‘steady-state infection’-like ecologies. Statistical co-occurrence examinations of the dsDNA, ssRNA and dsRNA markers within the data revealed a broad spectrum of statistically strong and significant virus-host relationships that included both known as well as novel interactions. Our approach offers a method for screening the diversity and dynamics of active viral infections in natural systems and develops links between viruses and their potential hosts in situ.SignificanceViruses are important partners in ecosystem scale ecology, yet their study to date is primarily limited to single virus-host infection models in the laboratory or limited to “potential-actions” derived from metagenomics analyses. Using metatranscriptomic sequences from polyadenylated-RNA selected samples, we have simultaneously captured information regarding eukaryotic diversity and active infection by viruses with dsDNA genomes, resulting in a statistical opportunity to predict “who is infecting whom”. This approach further provides concurrent insight regarding viruses with ssRNA and dsRNA genomes, capturing dynamics for the communities of viruses infecting single-celled eukaryotes. Given the central role of these plankton in global scale processes, our efforts result in a transformational step-forward regarding the study of in situ virus-host interactions.