Insight into Hyalomma anatolicum biology by comparative genomics analysis

Ticks belong to the arthropods, the most diverse terrestrial animals on earth. Dating back to the Cambrian period, arthropods evolved into two lineages, Chelicerata and Mandibulata. The latter further radiated into the Myriapoda and the Pancrustacea (composing the crustaceans and insects). The Chelicerates include Pycnogonida, Xiphosura and Arachnida, spiders and Acari (ticks and mites). Ticks (Acari: Ixodidae) are ectoparasites of major medical and veterinary significance, and are validated vectors of infectious agents of humans, domestic animals, and wildlife, which can cause direct damage to the host, including pyemia, toxicosis, and paralysis (Das and Sharma, 1991). Tick-borne diseases result in high morbidity and mortality of infected humans and animals (Kumar et al., 2020). Within the Order Ixodida, the majority of species are ectoparasites of major medical and veterinary significance, which potentially spread multiple pathogens responsible for serious diseases (e.g. Lyme borreliosis, anaplasmosis, babesiosis, ehrlichiosis, rickettsiosis, and CCHF (Luo et al., 2003, Guan et al., 2009, Li et al., 2010, Verma et al., 2011). Every year, approximately 300,000 cases of Lyme disease are reported in the United States (Shapiro and Wormser, 2018). Economic losses induced by management of ticks and tick-borne diseases have been estimated at approximately $30 billion per year (Lew-Tabor and Rodriguez Valle, 2016).

The ixodid tick species of the genus Hyalomma have drawn great attention, as they infest a wide range of hosts and transmit a great diversity of pathogens. Typically, Hyalomma anatolicum is widely distributed in Africa, Asia, and Europe, and can infest and transmit CCHF virus in humans, Theileria annulata and Theileria lestoquardi in cattle, Theileria equi in horses, Babesia sp. Xinjiang in sheep, Rickettsia, and viruses. CCHF is frequently reported throughout Africa, central Asia, southern Europe, the Middle East, and the Indian subcontinent. Between January and May 2022, over 200 cases of CCHF were documented by the World Health Organization (WHO) from Iraq (Sah et al., 2022). Furthermore, 1.7% of human blood samples (43/2,454) and 12.7% of samples from livestock were positive for CCHF virus in Xinjiang, China (Guo et al., 2017, Teng et al., 2022). The cost of control of tropical theileriosis has been estimated at ∼$240 million. Emerging and re-emerging tick-borne diseases and wide distribution of these diseases have caused serious issues for public health and husbandry industries. Completing the tick genome will provide a significant resource to aid understanding of tick biology, tick–pathogen and tick–host interactions, and control strategies.

The first tick genome provides valuable opportunities for understanding the adaptive evolution and parasitic features of Ixodes scapularis (Gulia-Nuss et al., 2016). Highly complete genomes of Dermacentor silvarum, Haemaphysalis longicornis, Hyalomma asiaticum, I. scapularis, Rhipicephalus sanguineus, and Rhipicephalus microplus illustrate their genetic complexity and inter-relationships between the genomic structure and geographic prevalence, environmental adaptation, and vector capability of these tick species (Jia et al., 2020b). The wide distribution of tick vectors is a great challenge for human and animal health. Global climate change and human activity may contribute to transmission of a species. During its long-term evolution, Hy. anatolicum has evolved multiple mechanisms for a wide source of blood feeding from distinct hosts, host detection, and hemoglobin digestion (Kumar et al., 2020). Completing the whole genome sequencing will enable researchers identifying gene families associated with blood feeding and digestion, and conserved mechanisms responsible for its wide spread and occupation of ecological niches. In this study, we sequenced the complete genome of Hy. anatolicum, which provides opportunities for comparative analyses of its parasitic features and exploration of control strategies.

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