A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors

Abstract

Although segmented and unsegmented RNA viruses are commonplace, the evolutionary links between these two very different forms of genome organization are unclear. We report the discovery and characterization of a tick-borne virus--Jingmen tick virus (JMTV)--that reveals an unexpected connection between segmented and unsegmented RNA viruses. The JMTV genome comprises four segments, two of which are related to the nonstructural protein genes of the genus Flavivirus (family Flaviviridae), whereas the remaining segments are unique to this virus, have no known homologs, and contain a number of features indicative of structural protein genes. Remarkably, homology searching revealed that sequences related to JMTV were present in the cDNA library from Toxocara canis (dog roundworm; Nematoda), and that shared strong sequence and structural resemblances. Epidemiological studies showed that JMTV is distributed in tick populations across China, especially Rhipicephalus and Haemaphysalis spp., and experiences frequent host-switching and genomic reassortment. To our knowledge, JMTV is the first example of a segmented RNA virus with a genome derived in part from unsegmented viral ancestors.

Keywords: evolution; segmentation.

Fig. 1.

Transmission EM image of JMTV in (A) infected cells and (B) cell culture supernatant. The viral particles are indicated by the orange arrowheads.

Fig. 2.

Schematic genome organization and putative proteomic maps of JMTV, showing predicted ORFs (blue boxes), transmembrane regions (yellow boxes), signal peptides (red box), and N-linked glycosylation sites (upward-pointing pink triangles).

Fig. 3.

ML phylogenetic trees of (A) NS3 and (B) NS5 proteins of JMTV and TCLA within the context of representative flaviviruses. The trees are midpoint-rooted, and all horizontal branches are drawn to a scale of amino acid substitutions per site. The branch and taxon labels of the JMTV–TCLA clade are shaded red. For clarity, bootstrap values are only shown for internal nodes.

Fig. 4.

ML phylogenetic trees of the four genome segments obtained from nine depooled JMTV samples. The trees are midpoint-rooted, and all horizontal branches are drawn to a scale of nucleotide substitutions per site. Major clade/lineages are shaded with blue, yellow, and red, respectively. Phylogenetic incongruence, suggestive of reassortment, is indicated with colored arrowheads.