Diverse and abundant viruses exploit conjugative plasmids

Abstract

Viruses exert profound evolutionary pressure on bacteria by interacting with receptors on the cell surface to initiate infection. While the majority of bacterial viruses, phages, use chromosomally-encoded cell surface structures as receptors, plasmid-dependent phages exploit plasmid-encoded conjugation proteins, making their host range dependent on horizontal transfer of the plasmid. Despite their unique biology and biotechnological significance, only a small number of plasmid-dependent phages have been characterized. Here we systematically search for new plasmid-dependent phages using a targeted discovery platform, and find that they are in fact common and abundant in nature, and vastly unexplored in terms of their genetic diversity. Plasmid-dependent tectiviruses have highly conserved genetic architecture but show profound differences in their host range which do not reflect bacterial phylogeny. Finally, we show that plasmid-dependent tectiviruses are missed by metaviromic analyses, showing the continued importance of culture-based phage discovery. Taken together, these results indicate plasmid-dependent phages play an unappreciated evolutionary role in constraining horizontal gene transfer.