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In this review, we ( a) describe the importance of an ecological framework for viral metagenomics ( b) review its implications for a suite of specific tools and approaches in viral metagenomics, including their limitations ( c) highlight the often-overlooked interactions of viruses with other viruses and ( d) address applications and research needs of viral metagenomics within an ecological framework. Moreover, applying an ecological framework to the use of viral metagenomics in areas of virology traditionally considered nonecological holds enormous promise for advancing virology and understanding the global roles viruses play. These high-throughput approaches have advanced our understanding of viral ecology by providing insights into the diversity, abundance, and functional potential of viruses associated with different environments ( 5, 6). Metagenomics is the study of nucleic acid sequences from a collection of entities in a sample, with viral metagenomics focusing on the nucleic acids of viruses within the sample. Viral metagenomics has revolutionized the field of virology by providing culture-independent methods to detect and characterize the vast diversity of viruses that cannot be cultured and isolated in a high-throughput manner ( 1– 4). We highlight specific fundamental research needs to capitalize on its potential and advance the field. An ecological framework in viral metagenomics stands poised to broadly expand our knowledge in basic and applied virology.

It provides a structure for the study of the diversity, distributions, dynamics, and interactions of viruses with one another, hosts, and the ecosystem, including interactions with abiotic factors. An ecological framework explicitly considers diverse variants of viruses in populations that make up communities of interacting viruses, with ecosystem-level effects. Here, we emphasize the implementation of an ecological framework in viral metagenomic studies to address questions in virology rarely considered ecological, which can change our perception of viruses and how they interact with their surroundings. Viral metagenomics has expanded our knowledge of the ecology of uncultured viruses, within both environmental (e.g., terrestrial and aquatic) and host-associated (e.g., plants and animals, including humans) contexts.