Functional and evolutionary characterization of potential auxiliary metabolic genes (AMGs) of the global RNA virome

Abstract

RNA viruses play an important role in regulating their host and global biogeochemical cycling, and auxiliary metabolic genes (AMGs) are one of the main pathways by which viruses regulate hosts metabolism. However, the AMGs encoded by global RNA viruses are largely unexplored. Here, we annotated RNA viral genomes and identified AMGs from recently published global RNA virome datasets. We found 274 AMGs encoded by 243 RNA viral genomes, which accounts for only 0.008% of all 3,216,257 genomes investigated. These AMGs span 25 functional categories, the most prevalent being translation, energy metabolism, membrane transport, transcription, replication and repair, and signal transduction. Unlike DNA viruses, RNA viruses tend to encode AMGs influencing the genetic and environments information processing of their hosts, with fewer AMGs linked to nutrient cycling, such as carbon and nitrogen metabolism. In addition, RNA viruses encoding these AMGs were taxonomically diverse, spanning five established phyla, the newly proposed phylum "Taraviricota" and fourteen LucaProt supergroups. Host prediction indicated that most of these RNA viruses encoding AMGs infect eukaryotes, while only a few of them, including Leviviricetes and Vidaverviricetes, infect prokaryotes. Interestingly, the potential host phylum for most of these RNA viruses were different from the likely source phylum of their AMGs, suggesting the possibility that these RNA viruses acquired AMGs from organisms outside their predicted host range. This study provides the first comprehensive analysis of AMGs from global RNA virome, which greatly expands our understanding of their function roles, evolutionary history and virus-host interactions.