The protist Aurantiochytrium limacinum possesses two mirusvirus-like genomic elements, one a circular episome (AurliV-1) and the other (AurliV-2) a chromosomal integrant. Here we show that genes in both genomes are expressed and virions containing mainly AurliV-1 DNA are produced under starvation conditions and when cells are cultured in standard growth medium. Of 67 AurliV-1-encoded proteins detected using proteomics, 48 are enriched under starvation conditions, including the structurally important major capsid and triplex proteins. Our results establish Aurantiochytrium as a model system for elucidating mirusvirus-host interactions and demonstrate persistent viral infection in a microbial eukaryote.