Marine algal viruses exhibit a high level of diversity, and closely related viruses targeting the same algal host species can stably coexist. Here we report an example of a single virus-host system concealing hidden complexity. We discovered two double stranded (ds) DNA viruses infecting the Arctic picophytoplankter Micromonas polaris coexisting in culture for over a decade. Genomic sequencing of the lysate originally characterized as MpoV-44T revealed that it comprises two distinct prasinoviruses with ~203-204 kb genomes (MpoV-44T.A and MpoV-44T.B), of which conserved regions only accounted for 36% (the nucleotide level). The viruses were subsequently separated and compared at both genomic and phenotypic levels. In dual infection studies using a single host strain under nutrient-replete conditions, MpoV-44T.A outcompeted MpoV-44T.B. Yet MpoV-44T.B-like viruses were more abundant than MpoV-44T.A-like ones in natural Arctic metagenomes. This apparent paradox may be explained by differences in host strain specificity and/or possible resilience to nutrient stress by MpoV-44T.B, which we hypothesize based on genomic data. This work unveils hidden virus diversity, illustrating that the dynamics of viral coexistence are not always easily predictable, and underscores the importance of studying the underlying mechanisms at play.
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