Viruses are the most abundant biological entities in the world's oceans, where they play important ecological and biogeochemical roles. Metagenomics is revealing new groups of eukaryotic viruses, although disconnected from known hosts. Among these are the recently described mirusviruses, which share some similarities with herpesviruses.1 50 years ago, "herpes-type" viral particles2 were found in a thraustochytrid member of the labyrinthulomycetes, a diverse group of abundant and ecologically important marine eukaryotes,3,4 but could not be further characterized by methods then available. Long-read sequencing has allowed us to connect the biology of mirusviruses and thraustochytrids. We sequenced the genome of the genetically tractable model thraustochytrid Aurantiochytrium limacinum ATCC MYA-1381 and found that its 26 linear chromosomes have an extraordinary configuration. Subtelomeric ribosomal DNAs (rDNAs) found at all chromosome ends are interspersed with long repeated sequence elements denoted as long repeated-telomere and rDNA spacers (LORE-TEARS). We identified two genomic elements that are related to mirusvirus genomes. The first is a ∼300-kbp episome (circular element 1 [CE1]) present at a high copy number. Strikingly, the second, distinct, mirusvirus-like element is integrated between two sets of rDNAs and LORE-TEARS at the left end of chromosome 15 (LE-Chr15). Similar to metagenomically derived mirusviruses, these putative A. limacinum mirusviruses have a virion module related to that of herpesviruses along with an informational module related to nucleocytoplasmic large DNA viruses (NCLDVs). CE1 and LE-Chr15 bear striking similarities to episomal and endogenous latent forms of herpesviruses, respectively, and open new avenues of research into marine virus-host interactions.

Department of Biochemistry and Molecular Biology Dalhousie University College Street Halifax NS B3H 4R2 Canada

Department of Ecology and Evolution Stony Brook University Nicolls Road Stony Brook NY 11794 USA

Faculty of Science Charles University Opletalova 110 00 Staré Město Czechia

School of Marine and Atmospheric Sciences Stony Brook University Nicolls Road Stony Brook NY 11794 USA

U S Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Cyclotron Road Berkeley CA 94720 USA

U S Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Cyclotron Road Berkeley CA 94720 USA; Department of Plant and Microbial Biology University of California Berkeley University Avenue Berkeley CA 94720 USA

U S Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Cyclotron Road Berkeley CA 94720 USA; HudsonAlpha Institute for Biotechnology Genome Way Northwest Huntsville AL 35806 USA

Curr Biol. 2023 Dec 4;33(23):R1234-R1235. doi: 10.1016/j.cub.2023.10.037. PubMed

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