Rapid Diversification of a Natural Heterosigma akashiwo Virus Population during a Host Bloom

Despite the ecological importance of viruses, our understanding of their evolutionary dynamics in natural environments remains limited. This gap is particularly pronounced for giant dsDNA viruses of the phyla Nucleocytoviricota and Mirusviricota. Knowledge on their population genetic dynamics is mostly derived from a small number of laboratory-based experiments, while patterns in nature are rarely observed. To overcome this limitation, we traced the genetic structure and transcription status of Heterosigma akashiwo virus (HaV) using high-frequency, time-resolved sampling during a host bloom in a coastal area of Japan by integrating cell counting, metabarcoding, and metagenomic and metatranscriptomic sequencing. The results obtained revealed that HaV dominated the giant virus community in most samples, with relative abundance up to 56%. Despite its high abundance, the HaV population exhibited a low level of microdiversity, but had a higher pN/pS ratio than other giant viruses in the study site. Microdiversity increased during the early sampling period, peaked mid-sampling, and decreased during the later period, consistent with rapid diversification during viral expansion, which may be driven by both in situ mutations and the succession of pre-existing minor variants. Several accessory genes, including a glycosyltransferase and an endonuclease, were highly expressed, providing functional evidence consistent with host interaction-driven selective pressure during the bloom. Collectively, these results indicate that HaV population dynamics during algal blooms are shaped by host-driven selection acting on standing genetic variations.