Marine viruses play a crucial role in microbial mortality, structuring their communities, and driving biogeochemical cycles. Although our knowledge of their diversity has been greatly expanded, the associations between viruses and microbial hosts, and the temporal dynamics of those pairs remain largely unknown. In this study, we leveraged a two-year monthly sampling in coastal waters of the South China Sea and employed metagenomics, metatranscriptomics, viromics to survey the seasonal dynamics of bacteriophages, eukaryotic viruses (giant viruses and the newly discovered mirusviruses) and RNA viruses. We further applied metagenomic Hi-C, a proximity-ligation-based method to improve the quality of metagenome-assembled genomes (MAGs) as well as to connect viruses with their hosts. We recovered a substantial of high-quality MAGs for both viruses and microbial hosts, revealing unexplored genomic diversity in the South China Sea. Diverse groups of viruses demonstrated distinct seasonal occurrence patterns, which were driven by factors such as temperature and nutrient availability. We successfully detected numerous virus-host pairs in natural microbial communities through metagenomic Hi-C and other cultivation-independent approaches, revealing narrow and broad host ranges in different viruses. Additionally, a large proportion of auxiliary metabolism genes were identified, which were associated with unique adaptation strategies in diverse viral groups. Our study advances understanding of ecological dynamics of virus-microbe communities and the underlying mechanisms in the ocean.
 

virus-host association,giant viruses,mirusviruses,RNA viruses,temporal dynamics,auxiliary metabolism gene