Phylogenetic proximity is a key driver of temporal succession of marine giant viruses in a five-year metagenomic time-series.

Nucleocytoplasmic large DNA viruses (NCLDVs), also called giant viruses, are widespread in marine systems and infect a broad range of microbial eukaryotes (protists). Recent biogeographic work has provided global snapshots of NCLDV diversity and community composition across the world's oceans, yet little information exists about the guiding "rules" underpinning their community dynamics over time. We leveraged a five-year monthly coupled metagenomic-viromic time-series to quantify the community composition of NCLDVs off the coast of Southern California and characterize their temporal population dynamics. NCLDVs were dominated by Algavirales (Phycodnaviruses, 59%) and Imitervirales (Mimiviruses, 36%). We identified clusters of NCLDVs with distinct classes of seasonal and nonseasonal temporal dynamics. Overall, NCLDV population abundances were often highly dynamic, showing strong seasonal signals. The Imitervirales group had the highest relative abundance in the more oligotrophic late summer and fall, while Algavirales did so in winter. Generally, closely related strains had similar temporal dynamics, suggesting that evolutionary history is an important driver of the temporal niche partition of marine NCLDVs. However, a few closely-related strains had drastically different seasonal dynamics, suggesting that while phylogenetic proximity often indicates ecological similarity, occasionally phenology can shift rapidly, possibly due to host-switching. We also identified distinct functional content and possible interactions of two major NCLDV orders with diverse eukaryotes in the study environment- revealing their putative hosts that include both primary producers and heterotrophic grazers. Together, our multiannual time-series study captures diverse temporal patterns among marine giant viruses and demonstrates that evolutionary history plays a key role in shaping their temporal niche partitioning.