Multi-level mosaicism shapes the evolution of small eukaryotic DNA viruses

Abstract

Eukaryote-infecting small dsDNA viruses, including those referred to as virophages, polintons, and their relatives, are major constituents of ecosystems across the globe as both agents of mortality and as integrated elements that shape host genome evolution. As the ubiquity of these viruses has become apparent, there have been efforts to organize their diversity into major lineages in order to better understand their biogeography, ecological impact, and evolution. Virophages, polintons, and polinton-like viruses were recently placed in the sub-phylum Polisuviricotina, though efforts to resolve relationships within this sub-phylum have been complicated by the vast diversity of these viruses and the existence of horizontal gene transfer between their genomes. To address these complications, we have used a gene profile occurrence based method of phylogenetic tree construction to aid in comparative genomic analysis of Polisuviricotina. We find that mosaicism is common within Polisuviricotina, in particular, reassociation of replication modules and morphogenic modules occurs throughout major Polisuviricotina groups. In addition to mosaic exchanges of full replication modules, we also observe extensive domain swapping within some replicases, indicating that mosaic recombination occurs on both the genome and subgenic level in these viruses. Analysis of individual replication modules suggests that they may be capable of some level of autonomous mobility, partially decoupling their evolution from the morphogenic module. This model helps explain the high levels of mosaicism in these viruses and has implications for the mechanisms through which small dsDNA viruses evolve.