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

Abstract

The emergence of previously unknown disease-causing viruses in mammals is in part the result of a long-term evolutionary process. Reconstructing the deep phylogenetic histories of viruses helps identify major evolutionary transitions and contextualizes the emergence of viruses in new hosts. We used a combination of total RNA sequencing and transcriptome data mining to extend the diversity and evolutionary history of the RNA virus order Articulavirales , which includes the influenza viruses. We identified instances of Articulavirales in the invertebrate phylum Cnidaria (including corals), constituting a novel and divergent family that we provisionally named the “Cnidenomoviridae.” We further extended the evolutionary history of the influenza virus lineage by identifying four divergent, fish-associated influenza-like viruses, thereby supporting the hypothesis that fish were among the first hosts of influenza viruses. In addition, we substantially expanded the phylogenetic diversity of quaranjaviruses and proposed that this genus be reclassified as a family—the “Quaranjaviridae.” Within this putative family, we identified a novel arachnid-infecting genus, provisionally named “Cheliceravirus.” Notably, we observed a close phylogenetic relationship between the Crustacea- and Chelicerata-infecting “Quaranjaviridae” that is inconsistent with virus–host codivergence. Together, these data suggest that the Articulavirales has evolved over at least 600 million years, first emerging in aquatic animals. Importantly, the evolution of the Articulavirales was likely shaped by multiple aquatic–terrestrial transitions and substantial host jumps, some of which are still observable today.

Ecoclimate drivers shape virome diversity in a globally invasive tick species

“…This suggests that the viruses carried by ticks may have a more equal opportunity to be involved in spill-over events, potentially favouring their successful establishment in multiple animal hosts. This finding could potentially explain the phenomenon of tick-borne viruses being more inclined to act as generalists in infecting vertebrate hosts, which results in their relatively higher genetic diversity compared to other arthropods, such as mosquitoes [ 43 , 44 ]. Furthermore, we observed that regions with higher virome diversity in ticks had a greater occurrence of tick-borne pathogen (TBP) infections, underscoring the public health significance of climate-induced changes in the tick virome.…”

Structural and functional analysis of the minimal orthomyxovirus-like polymerase of Tilapia Lake Virus from the highly diverged Amnoonviridae family

“…For PA, there is very low overall homology between the three full-length sequences (TiLV, Asotus1, Flavolineata), with the Zn1 binding residues being conserved but not the putative endonuclease ‘active’ site residues (Supplementary Note 9 ). Most recently, metagenomics of corals in addition to transcriptome mining has led to identification of a proposed new family, Cnidenomoviridae , within the Articulavirales order, which would now include at least four families: Orthomyxoviridae , Amnoonviridae , Quaranjaviridae , and Cnidenomoviridae 36 . Future analysis of additional sequences will undoubtedly shed more light on the evolution of Articulavirales polymerases.…”

Diversity, evolution, and emergence of fish viruses

“…It is now widely accepted that the ancient evolutionary ancestors of notable human pathogens, including influenza virus (i.e., the Orthomyxoviridae ), and SARS-CoV-2 (i.e., the Coronaviridae ) originated in aquatic species, including fish, broadly mirroring vertebrate host evolution over a period spanning more than 500 million years ( 1 , 3 , 134 , 135 ). Fish viruses typically form deep lineages on family-level viral phylogenies that depict a backbone of virus-host co-divergence over millions of years, albeit with regular occurrences of intra-class host-switching, including at the intra-class level ( 1 , 3 ).…”