Origins and Evolution of the Global RNA Virome

Yuri I. Wolf; Darius Kazlauskas; Jaime Iranzo; Adriana LucÍa-Sanz; Jens H. Kuhn; Mart Krupovic; Valerian V. Dolja; Eugene V. Koonin

The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/451740 doi: bioRxiv preprint ( Figure 2A ): a levivirus-like ancestor that, like the extant members of the Leviviridae, possessed 297 a capsid protein unrelated to SJR-CP (19, 52) gave rise to naked eukaryotic RNA replicons 298 known as "mitoviruses" and "narnaviruses". These replicons consist of a single RdRp gene (Fig. 299 2B) and replicate either in mitochondria or in the cytosol of the host cells, respectively, of fungal 300 and invertebrate hosts (the latter hosts were identified in metaviromic holobiont analyses) (14, 301 53) . Recently, the existence of plant "mitoviruses" has been reported although it is not known 302 whether these viruses reproduce in the mitochondria (54). The "narnavirus" RdRp is also the 303 ancestor of the RdRp of the expanding group of "ourmiaviruses" (Figure 2A ). "Ourmiaviruses" 304 were originally identified in a narrow range of plants, and genomic analysis revealed the 305 chimeric nature of these viruses, with a "narnavirus"-like RdRp but SJR-CPs and movement 306 proteins (MPs) which were apparently acquired from "picorna-like" and "tombus-like" viruses, 307 respectively (55). Use of metaviromics has led to the identification of numerous related viruses 308 associated with invertebrates, many of which encode distinct SJR-CP variants and some of which 309 acquired an RNA helicase ( Figure 2B and S2) (14) . Thus, the evolution of this branch apparently 310 involved the loss of the structural module of leviviruses, which yielded naked RNA replicons 311 that reproduced in the mitochondria of early eukaryotes. A group of these replicons subsequently 312 escaped to the cytosol which was followed by the reacquisition of unrelated structural modules 313 from distinct lineages of eukaryotic viruses inhabiting the same environment ( Figure 2B The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/451740 doi: bioRxiv preprint groups that were previously considered peripheral members of this supergroup, such as 320 totiviruses and nodaviruses, were relocated to different branches in the present tree (Branches 4 321 and 3, respectively), whereas the viruses of the order Nidovirales were moved inside Branch 2 322 from an uncertain position in the tree. Nevertheless, the core of the supergroup remains coherent, 323 suggestive of common ancestry. Within Branch 2, 3 major clades are strongly supported ( The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. recently evolved branch of partitiviruses is characterized by larger, 4-6-partite genomes, in 365 All rights reserved. No reuse allowed without permission.