Heterogeneous viromes in the salivary glands, ovaries, and midguts suggested differential viral transmission advantages of six tick genera.

UNLABELLED: The transmission of tick-borne viruses is associated with the biological functions of tick tissues. This study investigated the viromes in salivary glands, ovaries, and midguts collected from nine tick species of six genera and identified 49 viruses from at least 14 families. A variety of viral abundance and diversity across the three tissues was demonstrated. Ovaries of Rhipicephalus (Boophilus), Rhipicephalus, Dermacentor, and Hyalomma exhibited high viral abundance, suggesting their vertical transmission advantages, while high viral abundance observed in the salivary glands of Haemaphysalis and Ixodes indicated their advantage for horizontal transmission. Midguts of Rhipicephalus (Boophilus), Haemaphysalis, Dermacentor, and Ixodes exhibited high viral diversity, as did the salivary glands of Rhipicephalus and Hyalomma. Viruses found across the three tissues (tissue-common viruses) exhibited varied abundance (confirmed by qPCR), possessing a broad tissue spectrum but reflecting different tissue preferences. Viruses presenting high abundance identified in a single tissue (tissue-specific viruses) may be indicative of limited dissemination to other tissues. Furthermore, the correlation between viral abundance and tissues indicated distinct preliminary dissemination patterns of viruses across the examined tick genera. This study demonstrated the heterogeneity of viromes in tick tissues, revealed diverse viral preferences for tissues, and suggested the transmission advantages linked to specific tick genera. The findings provide novel insight into the differential competence of virus transmission in ticks, which raised the necessity of investigation and will benefit further research into the heterogeneous landscape of viromes within tick bodies and the mechanisms for maintaining and transmitting a particular virus in specific tick species.

IMPORTANCE: Tick tissues (salivary glands, ovaries, and midguts) are critical for the development of ticks and virus transmission. This study analyzed viromes in these tissues across six tick genera, thereby revealing the viral heterogeneity in tick tissues and suggesting differential transmission advantages among the examined genera. The results provide a novel insight into the understanding of the competence for virus transmission by ticks, based on viral populations, and into the mechanisms underlying virus dissemination within tick bodies, as well as those of vertical or horizontal transmission of viruses linked to the biological functions of tick tissues. The findings also suggest the importance of a more in-depth investigation into viral transmission, with a particular focus on the viromes of tick eggs, saliva, and hemolymph. All these would serve as a crucial foundational framework, establishing a robust foundation for the future development of strategies aimed at the control of viral transmission by ticks.