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G Yoshikawa, R Blanc-Mathieu, C Song, Y Kayama, T Mochizuki, K Murata, H Ogata and M Takemura
Abstract
Recent discoveries of new large DNA viruses reveal high diversity in their morphologies, genetic repertoires, and replication strategies. Here, we report the novel features of Medusavirus, a large DNA virus newly isolated from hot spring water in Japan. Medusavirus with a diameter of 260 nm shows a T=277 icosahedral capsid with unique spherical-headed spikes on its surface. It has a 381 kb genome encoding 461 putative proteins, 86 of which have their closest homologs in Acanthamoeba castellanii, whereas 279 (61%) are ORFans. The virus lacking the genes of DNA topoisomerase II and RNA polymerase showed that the DNA replication takes place in the host nucleus while the progeny virions are assembled in the cytoplasm. Furthermore, Medusavirus encoded all of five types of histones (H1, H2A, H2B, H3, and H4) and one DNA polymerase, which are phylogenetically placed at the root of the eukaryotic clades. By contrast, the host amoeba encoded many Medusavirus homologs including the major capsid protein. These facts strongly suggested that amoeba is indeed the most promising natural host of Medusavirus, and lateral gene transfers have taken place repeatedly and bidirectionally between the virus and its host since the early stage of their co-evolution. Medusavirus reflects the traces of direct evolutionary interactions between the virus and eukaryotic hosts, which may be caused by sharing the DNA replication compartment and evolutionarily long lasting viral-host relationships. Based on its unique morphological characteristics and phylogenomic relationships with other known large DNA viruses, we propose that Medusavirus forms a new family MedusaviridaeIMPORTANCE We have isolated a new NCLDV virus from hot spring water in Japan, named Medusavirus. This new NCLDV is phylogenetically placed at the root of the eukaryotic clades based on the phylogenies of several key genes including DNA polymerase, and surprisingly encodes the full set of histone homologs. Furthermore, its laboratory host, Acanthamoeba castellanii, encodes many Medusavirus homologs in its genome including the major capsid protein, suggesting that the amoeba is the genuine natural host of this new virus from ancient times, and lateral gene transfers have occurred between the virus and amoeba repeatedly. These results suggest that Medusavirus is a unique NCLDV preserving ancient footprints of evolutionary interactions with its hosts, thus providing clues to elucidate the evolution of NCLDVs, eukaryotes, and viral-host interaction. Based on the dissimilarities with other known NCLDVs, we propose that Medusavirus forms a new viral family Medusaviridae.
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