A Novel Rubi-Like Virus in the Pacific Electric Ray (Tetronarce californica) Reveals the Complex Evolutionary History of the Matonaviridae

Abstract

Rubella virus (RuV) is the causative agent of rubella ("German measles") and remains a global health concern. Until recently, RuV was the only known member of the genus Rubivirus and the only virus species classified within the Matonaviridae family of positive-sense RNA viruses. Recently, two new rubella-like matonaviruses, Rustrela virus and Ruhugu virus, have been identified in several mammalian species, along with more divergent viruses in fish and reptiles. To screen for the presence of additional novel rubella-like viruses, we mined published transcriptome data using genome sequences from Rubella, Rustrela, and Ruhugu viruses as baits. From this, we identified a novel rubella-like virus in a transcriptome of Tetronarce californica-order Torpediniformes (Pacific electric ray)-that is more closely related to mammalian Rustrela virus than to the divergent fish matonavirus and indicative of a complex pattern of cross-species virus transmission. Analysis of host reads confirmed that the sample analysed was indeed from a Pacific electric ray, and two other viruses identified in this animal, from the Arenaviridae and Reoviridae, grouped with other fish viruses. These findings indicate that the evolutionary history of the Matonaviridae is more complex than previously thought and highlights the vast number of viruses that remain undiscovered.

Keywords: Arenaviridae; Matonaviridae; Reoviridae; fish; metatranscriptomics; phylogeny; rubella; ruhugu; rustrela; virus discovery; virus evolution.

Figure 1

(a) Standardised abundance of viral reads (log) from the novel viruses (matonavirus, reovirus, and arenavirus) and a host gene (RPS13). (b,c) Phylogenetic trees of the non-structural and structural polyproteins of Tetronarce matonavirus within the Matonaviridae. (d) Phylogenetic tree of the L segment (RdRp) of Tetronarce arenavirus within the Arenaviridae. (e) Phylogenetic tree of segment 1 (RdRp) of Tetronarce reovirus within the Reoviridae. All phylogenetic trees are rooted at the midpoint. Viruses from fish species are highlighted within each phylogeny. Names of novel viruses identified in this study are in bold and highlighted. Nodes with bootstrap support values of >70% are indicated with asterisks (*).

Figure 2

Conserved sequence motifs between human Rubella virus (strain 1A), Rustrela virus (donkey), Ruhugu virus (bat), Tetronarce matonavirus, Tiger flathead matonavirus, and Guangdong Chinese water snake rubivirus shown. The non-structural (p200) polyprotein contains a conserved GDD amino acid motif in the p90 (RdRp) protein at positions 2313–2315. Regions corresponding to RuV B cell epitopes N1–N4 within E1 in the structural protein alignment at positions 1042–1116 are also illustrated. Bar graphs of percentage identity (%) of residues shown above the alignments with identities of 100% highlighted green. Genomic organisation of Matonaviridae (Rubella virus strain 1A) is shown below with segments able to be recovered from Tetronarce matonavirus and Guangdong Chinese water snake rubivirus indicated underneath for comparison. These comprise the complete structural polyprotein and partial non-structural polyproteins.