Double-stranded DNA viruses may serve as vectors for horizontal transfer of intron-generating transposons

Abstract

Specialized transposable elements capable of generating introns, termed introners, are one of the major drivers of intron gain in eukaryotes. Horizontal gene transfer (HGT) is thought to play an important role in shaping introner distributions. Viruses could function as vehicles of introner HGT since they often integrate into host genomes and have been implicated in widespread HGT in eukaryotes. We annotated integrated viral elements in diverse dinoflagellate genomes with active introners and queried viral elements for introner sequences. We find that 25% of viral elements contain introners. The vast majority of viral elements represent maverick-polinton-like double-stranded DNA (dsDNA) viruses as well as giant dsDNA viruses. By querying a previously annotated set of maverick-polinton-like proviruses, we show that introners populate full-length elements with machinery required for transposition as well as viral infection. Introners in the vast majority of viral elements are younger than or similar in age to others in their host genome, suggesting that most viral elements acquired introners after integration. However, a subset of viral elements show the opposite pattern wherein viral introners are significantly older than other introners, possibly consistent with virus-to-host horizontal transfer. Together, our results suggest that dsDNA viruses may serve as vectors for HGT of introners between individuals and species, resulting in the introduction of intron-generating transposons to new lineages.