Discovery and Characterization of TSPV1: A Spherical Archaeal Virus Decorated with Unusual Filaments

We describe the discovery of an archaeal virus, one that infects Archaea, tentatively named Thermoproteus spherical piliferous virus 1 (TSPV1), which was purified from a Thermoproteales host isolated from a hot spring in Yellowstone National Park (USA). TSPV1 packages an 18.65 Kb linear ds DNA genome coding for 31 ORFs, whose predicted gene products show little homology to known proteins. Comparison of virus particle morphologies and gene content demonstrate that TSPV1 is a new member of the Globulovirdae family of archaeal viruses. However, unlike other Globulovirdae members, TSPV1 has numerous highly unusual filaments decorating its surface, which can extend hundreds of micrometers from the virion. To our knowledge, similar filaments have not been observed in any other archaeal virus. The filaments are remarkably stable, remaining intact across a broad range of temperature and pH values, and are resistant to chemical denaturation and proteolysis. A major component of the filaments is a glycosylated 35 kDa TSPV1 protein (TSPV1 GP 24). The filament protein lacks detectable homology to structurally or functionally characterized proteins. We propose, given the low host cell densities of hot spring environments, that the TSPV1 filaments serve to increase the probability of virus attachment and entry into host cells.SignificanceHigh temperature environments have proven to be an important source for the discovery of new archaeal viruses with unusual particle morphologies and gene content. Our isolation of Thermoproteus spherical piliferous virus 1 (TSPV1), with numerous filaments extending from the virion surface, expands our understating of viral diversity and provides new insight into viral replication in high temperature environments.