Resolving deep evolutionary relationships within the RNA virus phylum <i>Lenarviricota</i>

Abstract

The RNA virus phylum <i>Lenarviricota</i> is composed of the fungi-associated families <i>Narnaviridae</i> and <i>Mitoviridae</i>, the RNA bacteriophage <i>Leviviridae</i>, and the plant and fungi-associated <i>Botourmiaviridae</i>. Members of the <i>Lenarviricota</i> are abundant in most environments and boast remarkable phylogenetic and genomic diversity. As this phylum includes both RNA bacteriophage and fungi- and plant-associated species, the <i>Lenarviricota</i> likely mark a major evolutionary transition between those RNA viruses associated with prokaryotes and eukaryotes. Despite the remarkable expansion of this phylum following metagenomic studies, the phylogenetic relationships among the families within the <i>Lenarviricota</i> remain uncertain. Utilising a large data set of relevant viral sequences, we performed phylogenetic and genomic analyses to resolve the complex evolutionary history within this phylum and identify patterns in the evolution of virus genome organisation. Despite limitations reflecting very high levels of sequence diversity, our phylogenetic analyses suggest that the <i>Leviviridae</i> comprise the basal lineage within the <i>Lenarviricota</i>. Our phylogenetic results also support the construction of a new virus family-the <i>Narliviridae-</i>comprising a set of diverse and phylogenetically distinct species, including a number of uniquely encapsidated viruses. We propose a taxonomic restructuring within the <i>Lenarviricota</i> to better reflect the phylogenetic relationships documented here, with the <i>Botourmiaviridae</i> and <i>Narliviridae</i> combined into the order <i>Ourlivirales</i>, the <i>Narnaviridae</i> remaining in the order <i>Wolframvirales</i>, and these orders combined into the single class, the <i>Amabiliviricetes</i>. In sum, this study provides insights into the complex evolutionary relationships among the diverse families that make up the <i>Lenarviricota</i>.