Giant endogenous viral elements in the genome of the model protist <i>Euglena gracilis</i> reveal past interactions with giant viruses

Genomes of giant viruses (phylum <i>Nucleocytoviricota</i>) have increasingly been found integrated into the genomes of diverse eukaryotes. Here, we report eight giant endogenous viral elements (GEVEs) in the genome of the microalgae <i>Euglena gracilis</i>. The GEVEs in <i>E. gracilis</i> bear signatures of genomic erosion, including invasion of transposable elements and duplications, suggesting that they are incapable of reactivation and virion production. Most of the GEVEs exhibit high average amino acid identity and cluster near each other in phylogenies of viral marker genes, suggesting that they are derived from the same ancestral viral lineage. Phylogenetic analysis of nucleocytovirus marker proteins reveals that the viruses belong to the order <i>Asfuvirales</i> in the same broader lineage that includes African swine fever virus, abalone asfarvirus, and giant viral sequences recently found in the fungus <i>Rhizophagus irregularis</i> and the marine gastropod <i>Elysia marginata</i>, suggesting that widespread host range transitions have occurred in this lineage. This work expands the diversity of known endogenous giant viruses and expands the host range of the <i>Asfuvirales</i> to include the superkingdom Discoba.IMPORTANCEThis study expands on the rapidly growing body of literature on the impact of latent giant viruses on eukaryotic genome evolution. In this study, we describe signatures of an understudied group of giant viruses integrated in the genome of <i>Euglena gracilis</i>, an ecologically and industrially relevant freshwater protist. The giant viruses in the genome of <i>Euglena</i> are relatives of important animal pathogens, such as African swine fever virus, which infects pigs, and abalone virus, which infects abalone. The broad range of hosts infected by this lineage of viruses exemplifies the impact of giant viruses on diverse eukaryotic lineages.