A survey of argasid ticks and tick-associated pathogens in the Peripheral Oases around Tarim Basin and the first record of Argas japonicus in Xinjiang, China

RESEARCH ARTICLE A survey of argasid ticks and tick-associated pathogens in the Peripheral Oases around Tarim Basin and the first record of Argas japonicus in Xinjiang, China Li Zhao1, Xiang-Mei Lin2, Fei Li1,3, Kai-Rui Li1, Bo He1, Lu-Yao Zhang1, Jiao-Jiao Pan1, Qiang-Rong Wang1, Jia-Min Gao1, Nicholas Johnson4, Xiang-Fen Yuan2, Ji-Zhou Lv2*, Shao-Qiang Wu2*, Yong-Hong Liu ID1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 College of Animal Science, Tarim University; Key Laboratory of Tarim Animal Husbandry Science and Technology of Xinjiang Production & Construction Corps, Alar, People’s Republic of China, 2 Institute of Animal Quarantine, Chinese Academy of Inspection and Quarantine, Beijing, People’s Republic of China, 3 Animal Loimia Controlling and Diagnostic Center of Aksu Region, People’s Republic of China, 4 Animal and Plant Health Agency, Woodham Lane, Surrey, United Kingdom * (Liu Y); (Wu S); (Lv J) OPEN ACCESS Citation: Zhao L, Lin X-M, Li F, Li K-R, He B, Zhang L-Y, et al. (2018) A survey of argasid ticks and tickassociated pathogens in the Peripheral Oases around Tarim Basin and the first record of Argas japonicus in Xinjiang, China. PLoS ONE 13(12): e0208615. https://doi.org/10.1371/journal. pone.0208615 Editor: Ben J Mans, Onderstepoort Veterinary Institute, SOUTH AFRICA Received: May 9, 2018 Accepted: November 20, 2018 Published: December 26, 2018 Copyright: © 2018 Zhao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The sequences of 12S rRNA of ticks obtained in this study were deposited in GenBank under accession numbers MG651960 to MG651967 and MG668793 to MG668795. The sequences of 16S rRNA of ticks obtained in this study were deposited in GenBank under accession numbers MG651950 to MG651959, and MH782636. Funding: This study was funded by National Natural Science Foundation of China (No. Abstract Argasid ticks (Acari: Argasidae) carry and transmit a variety of pathogens of animals and humans, including viruses, bacteria and parasites. There are several studies reporting ixodid ticks (Acari: Ixodidae) and associated tick-borne pathogens in Xinjiang, China. However, little is known about the argasid ticks and argasid tick-associated pathogens in this area. In this study, a total of 3829 adult argasid ticks infesting livestock were collected at 12 sampling sites of 10 counties in the Peripheral Oases, which carry 90% of the livestock and humans population, around the Tarim Basin (southern Xinjiang) from 2013 to 2016. Tick specimens were identified to two species from different genera by morphology and sequences of mitochondrial 16S rRNA and 12S rRNA were derived to confirm the species designation. The results showed that the dominant argasid ticks infesting livestock in southern Xinjiang were Ornithodoros lahorensis (87.86%, 3364/3829). Ornithodoros lahorensis was distributed widely and were collected from 10 counties of southern Xinjiang. Argas japonicus was collected from Xinjiang for the first time. In addition, we screened these ticks for tick-associated pathogens and showed the presence of DNA sequences of Rickettsia spp. of Spotted fever group and Anaplasma spp. in the argasid ticks. This finding suggests the potential role for Argas japonicus as a vector of pathogens to livestock and humans. Introduction Ticks could carry and transmit a variety of pathogens, including viruses, bacteria, rickettsiae, spirochetes, protozoans, chlamydia, mycoplasma and nematodes [1–4]. Two families of ticks are of medical significance: Ixodidae (hard ticks) and Argasidae (soft ticks). Argasid ticks PLOS ONE | https://doi.org/10.1371/journal.pone.0208615 December 26, 2018 1 / 13 A survey of argasid ticks and tick-borne pathogens 31460655 to LZ and No. 31860698 to Y.H.L.), and the National key research and development program of China (No. 2016YFD0501100 to SOW), and the open project of Key Laboratory of Tarim Animal Husbandry Science and Technology, Xinjiang Production & Construction Corps (HS201501 to YHL, HS201801 to LJZ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. comprise about 185 species from four genera. Approximately 19 species of Argasidae have been identified in China [5]. As the largest province of China, Xinjiang Uygur Autonomous Region covers over onesixth of the country’s territory, including the majority of the arid areas in the country [6]. Forty two species of ticks in 9 genera have been identified in Xinjiang, which represent more than 1/3 of total tick species found in China [7]. Six species of argasid ticks from two genera have been reported in Xinjiang, including Argas vespertilionis, Ar. persicus, Ar. reflexus, Ornithodoros lahorensis, Or. papillipes, and Or. tartakovskyi. The Tarim Basin is an endorheic basin, occupying an area of about 1,020,000 km2 [8]. It is sometimes used synonymously to refer to the southern half of the province, or southern Xinjiang. The vast territory, with complex geography, and diverse ecological environments within the Tarim Basin provides various habitats for argasid ticks [9]. Ninety percentage of humans and animals of Tarim Basin inhabit the Peripheral Oases, which are the most important ecosystems in the arid area [10]. Argasid ticks-livestock-humans interfaces in the Oases could promote the spread of tick-borne diseases. More importantly, previous studies have shown that a high prevalence of tick-borne pathogens exists in Xinjiang province, such as piroplasms, Anaplasma spp., Rickettsia spp. and Borrelia spp. [6, 11–13]. However, these studies focused on ixodid ticks and there have been few research regarding argasid ticks and assciated tick-borne pathogens. In the present study, the populations of argasid species associated with livestock at the sites around the Tarim Basin of Southern Xinjiang had been investigated. In addition, the presence of argasid tick-associated pathogens was assessed using molecular techniques. Materials and methods Sampling area, tick sampling and identification During the period from 2013 to 2016, we collected argasid tick specimens associated with livestock at twenty-seven sampling sites in Oases around the Tarim Basin of southern Xinjiang. This included farms at Aral, Artux, Awat, Hejing, Hetan, kargilik, Kuqa, Luntai, Makit, Minfeng, Pishan, Poskam, Qiemo, Qira, ShanShan, Shufu, Tumxuk, Tuokexun, Uqturpan, Wensu, Xayar, Xinhe, Yanqi, Yarkand, and Yopurga (Fig 1a). For the majority of counties, there was only one sampling site except Wensu county, which had three sampling sites. Each sampling site was examined for argasid ticks associated with livestock from January (...truncated)