Striking Tick-Borne Virus Diversity and Potential Reservoirs Documented During One-Health Cross-Sectional Screening in Anatolia

Abstract

An expansion of recently described human pathogenic tick-borne viruses from Central Asia toward Europe has been documented. Located on important bird migration routes, Anatolia is an intercontinental crossing hub with various climactic zones and with an abundance of endemic tick species. We sought to investigate tick-borne viruses utilizing a One Health approach encompassing host-removed ticks and host samples.MethodsWe collected host-attached ticks and accompanying plasma in 2023-2024 at locations in 20 provinces representing the 7 distinct geographical regions in Anatolia. The hosts comprised cattle, sheep, dogs, goats, and tortoises. The ticks were morphologically identified, processed in pools, and these pools, along with plasma from cattle, sheep and goats, were subjected to nucleic acid purification and complementary DNA synthesis. Viruses were screened by generic (nairovirus) and specific (Jingmen tick virus, JMTV; Tacheng tick virus 1, TcTV-1; Tacheng tick virus 2, TcTV-2; and Tamdy virus, TAMV) amplification assays and characterized by sequencing.ResultsA total of 93 animal plasma samples and 1265 samples from 11 tick species were screened in 192 pools. Crimean-Congo hemorrhagic fever virus (CCHFV) was detected in five tick species in ten pools (5.2%). Three distinct virus lineages, including Europe 1 and 2, as well as Africa 1, were noted. TcTV-1 was identified in 6 tick species in 12 pools (6.3%) and in a cattle plasma sample. Analysis of the nucleoprotein-encoding sequences revealed two separate virus clades, distinct from those reported from Asia and Europe. TAMV was identified in two tick species (1%). We further detected JMTV in 7 pools (3.6%), with sequences forming a new clade phylogenetically closer to viruses of Asian origin than local strains. Finally, highly divergent sequences of a novel nairovirus, forming a distinct group sharing ancestors with TcTV-1, TAMV, and pangolin/tick-associated nairoviruses, was observed in four pools (2%), comprising Haemaphysalis parva ticks.ConclusionsWe described a previously undocumented diversity of tick-borne viral pathogens, CCHFV, TcTV-1, and JMTV, in Anatolia. Possible animal reservoirs of TcTV-1 were identified. These pathogens and TAMV should be considered in the diagnostic workup of cases with symptoms associated with tick bites and in future surveillance efforts.