Large DNA viruses in early diverging fungal genomes are relics of past and present infections

Abstract

AbstractGiant viruses of the phylum Nucleocytoviricota have captured researchers’ attention due to their increasingly recognized impacts on eukaryotic genome evolution. Their origins are hypothesized to predate or coincide with the diversification of eukaryotes and their natural hosts span the eukaryotic tree of life. But surprisingly, giant viruses have not been found in the fungal kingdom, though recent metagenomic work suggests a putative association. Here we show that early-diverging fungal lineages maintain both “viral fossils” and host active infections by giant viruses, which form a monophyletic clade that we nameMycodnaviridae. Viral genomes described here span up to 350kb and encode over 300 genes, including many genes characteristic of giant viruses. Interestingly, we observed variation in infection status among the isolates including apparent active infection and transcriptionally-suppressed states, suggestive that viral activation may be constrained to certain life stages of the host. Our experimental findings add to the scant few natural virus-host systems available in culture for the study of giant viruses. These viruses have likely shaped the early evolution of these fungal lineages and should prove a useful model for their study.