Diversity and circulation of Jingmen tick virus in ticks and mammals

Abstract

Since its initial identification in ticks in 2010, Jingmen tick virus (JMTV) has been described in cattle, rodents, and primates. To better understand the diversity, evolution, and transmission of JMTV, we sampled 215 ticks, 104 cattle bloods, 216 bats, and 119 rodents in Wenzhou city, Zhejiang Province, China as well as 240 bats from Guizhou and Henan Provinces. JMTV was identified in 107 ticks (from two species), 54 bats (eleven species), 8 rodents (three species), and 10 cattle, with prevalence levels of 49.8, 11.8, 6.7, and 9.6 per cent, respectively, suggesting that bats may be a natural reservoir of JMTV. Phylogenetic analyses revealed that all the newly identified JMTVs were closely related to each other and to previously described viruses. Additionally, all tick and mammalian JMTV sampled in Wenzhou shared a consistent genomic structure, suggesting that the virus can cocirculate between ticks and mammals without observable variation in genome organization. All JMTVs sampled globally could be divided into two phylogenetic groups, Mantel tests suggested that geographic isolation, rather than host species, may be the main driver of JMTV diversity. However, the exact geographical origin of JMTV was difficult to determine, suggesting that this virus has a complex evolutionary history.

Keywords: Jingmen tick virus; diversity; evolution; mammals; ticks; transmission.

Figure 1.

A map of the world showing the location of the trap sites (red solid circle) in which ticks, bats, rodents, and cattle blood were sampled in China in this study, as well as the location of known JMTVs and their associated hosts (red hollow circle).

Figure 2.

A comparison of protein structures of representative tick and mammalian-associated JMTVs. The viruses recovered in this study are highlighted with bold. A unified length scale is used for all the proteins.

Figure 3.

Phylogenetic analysis of the nt sequences of four segments of JMTV. Because of the high sequence similarity of the JMTVs discovered in this study, representative sequences including six complete genomes (brown triangles) and nine nearly complete genomes (gray circles) were used to infer the evolutionary trees. The JMTVs containing three or four segments and available on GenBank were used as reference sequences. Phylogenetic groups, as well as host and geographical origin are indicated. The JMTV whose segment 4 encoded non–overlapping ORFs is marked with red stars in the segment 4 phylogenetic. All trees were rooted using Alongshan virus. Bootstrap values (>70%) are shown at relevant nodes. The scale bar represents the number of nt substitutions per site. The GenBank accession numbers of the viruses used in the trees are found in Supplementary Fig. 2.