Multiple waves of viral invasions in Symbiodiniaceae algal genomes

Abstract

Dinoflagellates from the family Symbiodiniaceae are phototrophic marine protists that engage in symbiosis with diverse hosts. Their large and distinct genomes show pervasive gene duplication and large-scale retroposition events. However, little is known about the role and scale of horizontal gene transfer (HGT) in the genomic evolution of this algal family. In other dinoflagellates, higher levels of HGTs have been observed, linked to major genomic transitions, such as the appearance of a viral acquired nucleoprotein that originated via HGT from a large DNA algal virus. Previous work showed Symbiodiniaceae from different hosts being actively infected by several viral groups, such as giant DNA viruses and ssRNA viruses, that may play an important role in coral health. This includes a hypothetical latent viral infection, whereby viruses could persist in the cytoplasm or integrate into the host genome as a provirus. This hypothesis received some experimental support however, the cellular localization of putative latent viruses and their taxonomic affiliation are still unknown. In addition, despite the finding of viral sequences in some genomes of Symbiodiniaceae, viral origin, taxonomic breadth, and metabolic potential have not been explored. To address these questions, we searched for evidence of protein sequences of putative viral origin in 13 Symbiodiniaceae genomes. We found 59 candidate viral-derived HGTs that give rise to 12 phylogenies across 10 genomes. We also describe the taxonomic affiliation of these virus-related sequences, their structure, and genomic context. These results lead us to propose a model to explain the origin and fate of Symbiodiniaceae viral acquisitions.