Emerging tick-borne viruses are posing an increasing health concern. However, there is limited knowledge about the distribution characteristics of tick virome in Yunnan Province, southwestern China, where it is distinguished by its diverse eco-climatic zones and rich biodiversity, making it a hotspot for studying tick-borne pathogens. The present study aimed to explore the diversity and ecological characteristics of tick virome in Yunnan Province, especially to identify novel potentially pathogenic viruses threatening human and vertebrate animals, and to investigate host-specific viral tropisms and their transmission characteristics. Using a meta-transcriptomic approach, the study analyzed the viromes of 448 individual ticks and approximately 10,000 eggs collected from nine counties with different hosts, altitudes and landscapes. The ticks encompassed eight species across four genera. The study focused on delineating virome diversity profiles, evaluating host-specific viral tropisms, and investigating potential transovarial transmission through viral contigs identification and Sanger sequencing. The study identified 53 viral families, revealing significant virome diversity and geographic and environmental specificity. Haemaphysalis and Ixodes ticks exhibited greater viral richness and abundance, with host taxonomy being a primary influencing factor. We determined 102 viral genomes encompassing 35 species, comprising 15 novel viruses identified when their RNA-dependent RNA polymerase/DNA polymerase sequences exhibited <90% amino acid identity to known viruses. The novel vectors for vertebrate-related or potentially pathogenic viruses were also detected, thus providing new insights into transmission cycles. The evidence for transovarial transmission was reinforced by the absence of significant differences in Chuviridae and Nairoviridae families between female ticks and their eggs. These findings underscore the necessity of continuous surveillance to avert the spillover of emerging pathogens.
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