Virome of Hyalomma and Rhipicephalus ticks from desert of Northwestern China

Abstract

Ticks are important vectors for pathogen transmission, yet studies on the diversity and distribution of viruses carried by ticks in desert regions remain limited. This study investigated the tick virome in desert areas of Xinjiang, China, and identified two tick species, Hyalomma asiaticum and Rhipicephalus turanicus. A total of 30 meta-transcriptome sequencing libraries were constructed from ticks pooled by location, tick species, sex, and host. The proportion of viral reads ranged from 0.004% to 0.165%, and significant differences in viral alpha- and beta-diversity were observed between the two tick species. A total of 125 complete or nearly complete viral genomes were classified into 5 families of positive-sense single-stranded RNA viruses, 6 families of negative-sense single-stranded RNA viruses, and 2 families of double-stranded RNA viruses. Twenty-eight viral species were identified, including 20 known viruses and 8 novel viruses from the genera Orthonairovirus, Quaranjavirus, and Mitovirus, and families Peribunyaviridae and Narnaviridae. Notably, the discovery of Desert orthonairovirus, Desert quaranjavirus, and Desert peribunya-like virus revealed a potential new role for desert ticks as viral vectors. Among the other 25 viruses, 12 were specific to H. asiaticum, and 9 were specific to R. turanicus. This study highlights the diversity of tick-borne viruses in Xinjiang's desert regions, their distribution across different tick species, and underscores the importance of these tick species in pathogen transmission. These findings provide scientific evidence for further research into viral circulation in desert ecosystems and the potential public health threats posed by tick-borne pathogens.

Keywords: Hyalomma asiaticum; Rhipicephalus turanicus; desert; emerging tick-borne virus; tick virome.

Figure 1.

Virus diversity between H. asiaticum and R. turanicus. (a) Relative abundance profile of viruses between H. asiaticum and R. turanicus. Each cell in the heat map represents the normalized number of reads belonging to the viral family. (b) Comparison of alpha-diversity of tick viromes (Shannon index) between H. asiaticum and R. turanicus. Boxplot elements: center line, median; box limits, upper and lower quartiles; whiskers (error bars), the highest and lowest points within 1.5 interquartile range of the upper and lower quartiles. The P-value was calculated using a two-sided Student’s t-test. (c) Between-group clustering of viromes between H. asiaticum and R. turanicus by PCoA. Presented according to axes 1 (14.56%) and 2 (20.78%).

Figure 2.

Phylogenetic trees constructed on the RdRp protein for RNA viruses. Newly identified viruses in this study were labelled with triangle; known viruses were labelled with solid circles. Viruses derived from H. asiaticum were represented in orange, while those from R. turanicus were indicated in blue.

Figure 3.

Phylogenetic analysis of vertebrate-associated ssRNA(−) viruses. (a) Phylogeny of viruses in the family Peribunyaviridae based on the RdRp protein. (b) Phylogeny of viruses in the genus Orthonairovirus based on the RdRp protein. (c) Genomic organization and putative CDSs of Desert orthonairovirus. The large (L) segment encodes L protein, the medium (M) segment encodes glycoprotein precursor (GPC), and the small (S) segment encodes nucleoprotein (N). (d) Phylogeny of viruses in the genus Quaranjavirus based on the RdRp protein. (e) Genome structure of Desert quaranjavirus and other quaranjaviruses. PB2, polymerase basic protein 2; PB1, polymerase basic protein 1; PA, polymerase acid protein; NP, nucleoprotein; HA, hemagglutinin protein; M, matrix protein; VP7, viral protein. (f) The terminal sequences of Desert quaranjavirus and other quaranjaviruses. The typical terminal sequences of Desert quaranjavirus and other quaranjaviruses are marked with boxes.

Figure 4.

Phylogenetic analysis of H. asiaticum-specific viruses. (a) Phylogeny of viruses in the genus Mitovirus based on the RdRp protein. (b) Phylogeny of viruses in the family Narnaviridae based on the RdRp protein. (c) Phylogeny of M. boleense based on the RdRp gene. (d) Phylogeny of Bole Tick Virus 1 based on the RdRp gene. (e) Phylogeny of A. bole based on the RdRp gene. (f) Phylogeny of viruses in the order Ghabrivirales based on the RdRp protein.

Figure 5.

Phylogenetic analysis of R. turanicus-specific viruses. (a) Phylogeny of viruses in the genus Mitovirus based on the RdRp protein. (b) Phylogeny of viruses in the family Botourmiaviridae based on the RdRp protein. (c) Phylogeny of Neofusicoccum parvum narnavirus 2 based on the RdRp gene. (d) Phylogeny of Hebei mivirus 1 based on the RdRp gene. (e) Phylogeny of Brown dog tick phlebovirus 1 based on the RdRp gene. (f) Phylogeny of Tick phlebovirus based on the RdRp gene.

Figure 6.

Phylogenetic analysis of shared ssRNA(+) viruses between two tick species. (a) Phylogeny of Botourmiaviridae sp. based on the RdRp protein. (b) Phylogeny of viruses in the family Mitoviridae based on the RdRp protein. (c) Phylogeny of U. alar1 based on the RdRp gene. (d) Phylogeny of Bole tick virus 4 based on the RdRp gene. (e) The comparison between Bole tick virus 4 detected in different tick species. Sequences derived from H. asiaticum were marked in an orange box, while that from R. turanicus were marked in a blue box.