Evidence for an aquatic origin of influenza virus and the orderArticulavirales

Abstract

The emergence of novel disease-causing viruses in mammals is part of the long evolutionary history of viruses. Tracing these evolutionary histories contextualises virus spill over events and may help to elucidate how and why they occur. We used a combination of total RNA sequencing and transcriptome data mining to extend the diversity and evolutionary history of the order Articulavirales, which includes the influenza viruses. From this, we identified the first instance of Articulavirales in the Cnidaria (including corals), constituting a novel and divergent family that we tentatively named the Cnidenomoviridae. This may be the basal group within the Articulavirales. We also extended the known evolutionary history of the influenza virus lineage by identifying a highly divergent, sturgeon-associated influenza virus. This suggests that fish were among the first hosts of influenza viruses. Finally, we substantially expanded the known diversity of quaranjaviruses and proposed that this genus be reclassified as a family (the Quaranjaviridae). We find evidence that vertebrate infecting Quaranjaviridae may have initially evolved in crustaceans before spilling into terrestrial Chelicerata (i.e., ticks). Together, our findings indicate that the Articulavirales has evolved over at least 600 million years, first emerging in aquatic animals. Importantly, the evolution of this order was not shaped by strict virus-host codivergence, but rather by multiple aquatic-terrestrial transitions and substantial host jumps, some of which are still observable today.

Host adaptive radiation is associated with rapid virus diversification and cross-species transmission in African cichlid fishes

“…Teleost fishes, the largest clade of living vertebrates that display extensive ecological diversity, are among those groups that naturally exhibit highly diverse viromes, making them an informative model system for determining the host and virological factors that impact crossspecies virus transmission 10,11 . Indeed, relatives of coronaviruses, hepatitis C virus, influenza viruses, filoviruses, and paramyxoviruses have all been identified in teleosts 2,[10][11][12][13][14][15] .…”

Current trends in RNA virus detection through metatranscriptome sequencing data

“…Essentially, the evolution of RNA viruses that cause human disease is complex because various RNA viruses that infect humans are not limited to mammals, but closely related RNA viruses also exist in fish [ 7 ]. Indeed, a recent study revealed fish could be the first host of the genus influenza virus that also infects humans [ 35 ]. Further RNA virome studies will reveal the diversity and evolution of RNA viruses that cause human diseases, including SARS‐CoV‐2.…”

Evidence for an ancient aquatic origin of the RNA viral order Articulavirales

“…The sequence accessions for the viruses identified here through data mining are provided in SI Appendix . The multiple sequence alignments used to generate all of the phylogenetic trees presented in this study are freely available at https://github.com/mary-petrone/ancient_articulavirales ( 56 ).…”