A type IV pili-mediated mutualism between two co-resident temperate archaeal viruses and their host

Co-resident temperate viruses are ubiquitous in prokaryotes, which interact with each other and affect their shared host. However, how such virus-virus and virus-host interactions play out in Archaea remains largely unexplored. Here, we discover a tripartite mutualistic interaction among the co-existing temperate viruses SNJ1 and SNJ2 and their host, haloarchaeon Natrinema sp. J7. We find that the SNJ2 provirus encodes two type IV pilins (T4Ps), which hijack the host secretion machinery to assemble into distinct filaments on the host cell surface. The SNJ2-encoded pili are dispensable for the SNJ2 infection but serve as receptors for SNJ1. As a quid pro quo, SNJ1 enhances the replication of SNJ2. Furthermore, the viral pili are the dominant filaments on the cell surface and promote biofilm formation and motility of the host. A number of SNJ2-like proviruses harbor T4P genes, suggesting that T4P-mediated virus-virus and virus-host interactions are widespread in Haloarchaea.