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The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. In contrast, virion architectures vary dramatically even within each of the three lineages of 413 the "alphavirus supergroup". The major structural themes include: variants of icosahedral capsids 414 formed by SJR-CP (e.g., bromoviruses, tymoviruses); unrelated icosahedral capsids enveloped in 415 a lipoprotein bilayer (togaviruses); flexuous filamentous capsids formed by a distinct type of CP 416 (alphaflexiviruses, betaflexiviruses, gammaflexiviruses, closteroviruses); and rigid rod-shaped 417 capsids assembled from another distinct CP (benyiviruses, virgaviruses). It was traditionally 418 thought that the latter capsid type is specific to viruses of flowering plants (20). However, the 419 recent discovery of a virgavirus-like CP in invertebrate viruses (e.g., Běihǎi charybdis crab virus 420 1 in Figure 4B ) (14) suggests that the emergence of this unique CP fold antedates land The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. . https://doi.org/10.1101/451740 doi: bioRxiv preprint Within Branch 3, the phylogenetically compact alphavirus supergroup is embedded within 433 the radiation of diverse virus groups including the well-known tombusviruses and nodaviruses, 434 along with several newcomers discovered via metaviromics, such as the "statovirus", "wèivirus", 435 "yà nvirus", and "zhà ovirus" groups (14, 80, 81) ( Figure 4A ). Our RdRp analysis revealed 436 remarkable phylogenetic heterogeneity within and among these groups and split "tombus-like 437 viruses" into 5 lineages with distinct evolutionary affinities (groups 'Uncl. inv.', and subsets of 438 "tombus-like viruses" and "nodaviruses" in Figure 4A ). This subdivision is also supported by the 439 analysis of the CPs of these viruses (see section on SJR-CP evolution; Fig. 7 ). Therefore, in 440 contrast to the alphavirus supergroup, nodaviruses or flavivirus supergroup, the term 'tombus-441 like' loses its evolutionary and taxonomic coherence. Accordingly, we use the term 442 "tombusviruses" (without quotation marks) only for one lineage that includes the members of the 443 current family Tombusviridae along with a broad variety of related plant and invertebrate 444 holobiont viruses (14) . 445