Metagenomic evidence of viral secretion from tick salivary glands to saliva: implications for potential horizontal transmission

Ticks transmit diverse viral pathogens to hosts during blood-feeding via saliva secretion. This study characterized viral compositions in salivary glands and saliva from adults of four tick species (Ixodes persulcatus, Rhipicephalus microplus, Haemaphysalis longicornis, and Haemaphysalis concinna) collected in China. Meta-transcriptomic analysis revealed distinct viromes across species, with Flaviviridae dominant in R. microplus, Nairoviridae in H. concinna and I. persulcatus, and Phenuiviridae in H. longicornis and I. persulcatus. Among 27 viruses detected in salivary glands, 14 were identified in saliva, indicating horizontal transmission potential. Viruses with higher abundance (transcripts per thousand bases per million, TPM) in salivary glands were more likely to be secreted in saliva. Genomic sequences of eight viruses, including severe fever with thrombocytopenia syndrome virus (SFTSV), tick-borne encephalitis virus (TBEV), Jingmen tick virus (JMTV), Songling virus (SGLV), Wetland virus (WELV), Beiji nairovirus (BJNV), Mukawa virus (MKWV), and Wuhan tick virus 2 (WHTV2), which are associated with human diseases or possess spillover potentials, were fully assembled from salivary glands and confirmed in saliva. Notably, SFTSV in H. longicornis; MKWV, Sichuan tick hepe-like virus, and Jilin luteo-like virus 2 in I. persulcatus; and JMTV in R. microplus showed significantly increased abundance in saliva, indicating an enhanced secretion of these viruses into saliva. Conversely, TBEV, BJNV, and Sara tick phlebovirus in I. persulcatus, SGLV and WELV in H. concinna, and WHTV2 in R. microplus exhibited reduced salivary abundance despite glandular presence. These findings demonstrate differential secretion capabilities of tick-borne viruses (TBVs) from glands to saliva, advancing understanding of horizontal transmission risks for pathogens affecting human health.