Marine Autographiviridae phages exhibit high genetic diversity and global-scale biogeographic patterns

Marine viral communities harbor an astounding diversity of phages infecting diverse marine bacteria. The double-stranded DNA phage family Autographiviridae is among the most abundant phage families in the ocean. However, the current understanding of marine Autographiviridae phages is predominantly derived from isolates infecting cyanobacteria, SAR11, and Roseobacter. To achieve a more comprehensive understanding of the diversity, ecological traits, and functional profiles of this phage family, we recovered 1253 complete marine Autographiviridae uncultivated viral genomes (UViGs). Comparative genomic analysis showed that marine-derived Autographiviridae phages display genome synteny and share a conserved core of seven genes. The core gene-based phylogenomic analysis classified them into 14 groups, 6 of which were previously undescribed. These groups varied in G + C content, genome size, and presence of specific genes. Metagenomic recruitment analysis demonstrated that Autographiviridae phages are globally distributed and enriched in the upper ocean layers of tropical and temperate zones. The differential distribution patterns among these groups mirror the ecological niches of their potential hosts, emphasizing the top-down control these phages exert on their host populations. Collectively, our study substantially expands knowledge regarding the diversity, potential hosts, functional capacity, and ecological distribution of Autographiviridae phages in the ocean, emphasizing their ecological implications in marine environments.