Global diversity of terrestrial Mirusviruses reveals host expansion to Archaea

Mirusviruses represent a deep evolutionary lineage of DNA viruses, proposed to bridge the viral realms of Duplodnaviria and Varidnaviria. Previously considered to be strictly aquatic viruses infecting unicellular eukaryotes, their full host range and ecological scope have remained enigmatic, thus limiting our understanding of their role in the tree of life. Here, through a global metagenomic survey across 24 terrestrial and aquatic ecosystems, we uncover the hidden diversity and evolutionary breadth of mirusviruses. We reveal that mirusviruses are not confined to aquatic environments but also abundant and diverse in terrestrial biomes, forming novel, deeply-branching phylogenetic lineages. Strikingly, convergent evidence from CRISPR-spacer matches and viral footprints in host genomes suggests that mirusviruses cross the domain boundary, infecting not only eukaryotes but also archaea across ten different phyla. This discovery fundamentally redefines mirusviruses as cross-domain viruses and provides compelling support for the 'mirusvirus origin' hypothesis, which posits their evolutionary origin to predate that of nucleocytoviruses. Our findings place mirusviruses at the nexus of ancient virus-host evolutionary dynamics, suggesting they served as ancestral hubs for cross-domain gene exchange at the dawn of eukaryogenesis.