Persistent mirusvirus infection in the marine protist Aurantiochytrium

Mirusviruses are enigmatic double-stranded (ds) DNA viruses with a chimeric evolutionary history – they have informational genes of Nucleocytoviricota ancestry and virion module genes most like those of herpesviruses. Mirusvirus genomes were discovered in marine metagenomic data (1) but, despite their abundance and broad environmental distribution, their host range is unknown. The marine thraustochytrid protist Aurantiochytrium limacinum was recently found to possess two mirusvirus-like genomic elements, one a circular episome (AurliV-1) and the other (AurliV-2) a chromosomal integrant (2). Here we show that A. limacinum mirusvirus genes are expressed and virions are produced in all culture conditions examined, including standard growth medium. Of 66 AurIiV-1-encoded proteins detected using proteomics, 48 were up-regulated under starvation conditions, including major capsid protein and triplex proteins. Quantitative PCR showed that AurliV-1 DNA is packaged into virions, and transmission electron microscopy revealed ~140 nm virions in the nucleus, in cytoplasmic vesicles, between the plasma membrane and cell wall, and in the extracellular environment. Putative surface-localized, AurliV-1-encoded, arylsulfatase and alpha-galactosidase proteins may digest sulfated polysaccharides in the host cell wall. Our results establish Aurantiochytrium as the first model system for elucidating mirusvirus-host interactions and reframe the concept of persistent viral infection in microbial eukaryotes.