Genome-resolved year-round dynamics reveal a broad range of giant virus microdiversity

Giant viruses are crucial for marine ecosystem dynamics because they regulate microeukaryotic community structure, accelerate carbon and nutrient cycles, and drive the evolution of their hosts through co-evolutionary processes. Previously reported long-term observations revealed that these viruses display seasonal fluctuations in abundance. However, the underlying genetic mechanisms driving such dynamics of these viruses remain largely unknown. In this study, we investigated the dynamics of giant viruses using time-series metagenomes from eutrophic coastal seawater samples collected over 20 months. A newly developed computational pipeline generated 1,065 high-quality genomes covering six major giant virus lineages. These genomic data revealed year-round recovery of the viral community structure at the study site and distinct dynamics of viral populations that were classified as persistent (n = 9), seasonal (n = 389), sporadic (n = 318), or others. By profiling the intra-species nucleotide-resolved microdiversity through read mapping, we also identified year-round recovery dynamics at subpopulation level for viruses classified as persistent or seasonal. Our results further indicated that giant viruses with broader niche breadth tended to exhibit higher levels of microdiversity. We argue that greater microdiversity of viruses likely enhances adaptability and thus survival under the virus-host arms race during prolonged interactions with their hosts.IMPORTANCERecent genome-resolved metagenomic surveys have uncovered the vast genomic diversity of giant viruses, which play significant roles in aquatic ecosystems by acting as bloom terminators and influencing biogeochemical cycles. However, the relationship between the ecological dynamics of giant viruses and underlying genetic structures of viral populations remains unresolved. In this study, we performed deep metagenomic sequencing of seawater samples collected across a time-series from a coastal area in Japan. The results revealed a significant positive correlation between microdiversity and temporal persistence of giant virus populations, suggesting that population structure is a crucial factor for adaptation and survival in the interactions with their hosts.