A filamentous archaeal virus is enveloped inside the cell and released through pyramidal portals

Significance Egress of most eukaryotic enveloped viruses, including such human pathogens as HIV-1, Ebola, and coronaviruses, occurs via budding through cellular membranes, a process concomitant with virion assembly. Archaea are also infected by enveloped viruses, but how their virions are assembled and released from the cells remained largely unknown. We show that virions of Sulfolobus islandicus filamentous virus (SIFV) are assembled and enveloped in the cell cytoplasm. Instead of budding, SIFV induces the formation of pyramidal structures, which penetrate the cell envelope and serve as portals for virion release. Comparison of the infection cycles of evolutionarily related enveloped and nonenveloped filamentous archaeal viruses suggests that the primary role of the lipothrixvirus membrane is to protect the genome against extreme environmental conditions.