Abstract
Viruses infecting archaea play significant ecological roles in marine ecosystems through host infection and lysis, yet they have remained an underexplored component of the virosphere. In this study, we recovered 451 archaeal viruses from a subtropical estuary, identifying 63 that are associated with the dominant marine order Poseidoniales (Marine Group II Archaea). Phylogenetic analyses of a subset of complete and nearly‐complete viral genomes assigned these viruses to the order Magrovirales , a lineage of Poseidoniales viruses, and identified a novel group of viruses distinct from Magrovirales . Utilising demarcation criteria established for the classification of archaeal tailed viruses, we propose two families within the order Magrovirales: Apasviridae (magrovirus group A), comprising the genera Agnivirus and Savitrvirus, and Krittikaviridae (magrovirus group E) encompassing the genus Velanvirus. Additionally, we propose a new order, distinct from Magrovirales , named Adrikavirales, which includes the genus Vyasavirus. Our detailed genomic characterisation of the new viral lineages revealed genes involved in viral assembly and egress, such as those responsible for creating holin rafts to lyse host cell membranes, a feature predominantly known from bacteriophages. Furthermore, we identified a broad spectrum of auxiliary metabolic genes, suggesting that these viruses can modulate host metabolism. Collectively, our findings substantially enhance the current understanding of the diversity and functional potential of Poseidoniales viruses.