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Viral RNA Metagenomics of Hyalomma Ticks Collected from Dromedary Camels in Makkah Province, Saudi Arabia

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Viral RNA Metagenomics of Hyalomma Ticks Collected from Dromedary Camels in Makkah Province, Saudi Arabia viruses Article Viral RNA Metagenomics of Hyalomma Ticks Collected from Dromedary Camels in Makkah Province, Saudi Arabia Fathiah Zakham 1,2,3,*,† , Aishah E. Albalawi 4 , Abdullah D. Alanazi 5 , Phuoc Truong Nguyen 1 , Abdulaziz S. Alouffi 6 , Altaf Alaoui 7 , Tarja Sironen 1,2 , Teemu Smura 1,8 and Olli Vapalahti 1,2,8 1 Department of Virology, Faculty of Medicine, University of Helsinki, 00014 Helsinki, Finland; phuoc.truong@helsinki.fi (P.T.N.); tarja.sironen@helsinki.fi (T.S.); teemu.smura@helsinki.fi (T.S.); olli.vapalahti@helsinki.fi (O.V.) 2 Department of Veterinary Biosciences, Faculty of Veterinary Medicine, University of Helsinki, 00014 Helsinki, Finland 3 Faculty of Pharmacy, University of Helsinki, 00014 Helsinki, Finland 4 Department of Biology, Faculty of Science, University of Tabuk, Tabuk 47912, Saudi Arabia; [email protected] 5 Department of Biological Sciences, Faculty of Science and Humanities, Shaqra University, Ad Dawadimi 11911, Saudi Arabia; [email protected] 6 King Abdulaziz City for Science and Technology, Riyadh 12354, Saudi Arabia; aaloufi@kacst.edu.sa 7 Laboratory of Engineering Sciences and Modeling, Ibn Tofail University, Kenitra 14000, Morocco; [email protected] 8 HUS Diagnostic Center, HUSLAB, Hospital District of Helsinki and Uusimaa, 00260 Helsinki, Finland * Correspondence: fathiah.zakham@helsinki.fi † Current address: Department of Virology, Medicum, POB 21 (Haartmaninkatu 3), University of Helsinki, 00014 Helsinki, Finland. Citation: Zakham, F.; Albalawi, A.E.; Alanazi, A.D.; Truong Nguyen, P.; Abstract: Arthropod-borne infections are a medical and economic threat to humans and livestock. Alouffi, A.S.; Alaoui, A.; Sironen, T.; Over the last three decades, several unprecedented viral outbreaks have been recorded in the Western Smura, T.; Vapalahti, O. Viral RNA part of the Arabian Peninsula. However, little is known about the circulation and diversity of Metagenomics of Hyalomma Ticks arthropod-borne viruses in this region. To prepare for new outbreaks of vector-borne diseases, it Collected from Dromedary Camels in is important to detect which viruses circulate in each vector population. In this study, we used a Makkah Province, Saudi Arabia. metagenomics approach to characterize the RNA virome of ticks infesting dromedary camels (Camelus Viruses 2021, 13, 1396. https:// dromedaries) in Makkah province, Saudi Arabia. Two hundred ticks of species Hyalomma dromedarii doi.org/10.3390/v13071396 (n = 196) and Hyalomma impeltatum (n = 4) were collected from the Alkhurma district in Jeddah and Al-Taif city. Virome analysis showed the presence of several tick-specific viruses and tick-borne Academic Editor: Subir Sarker viruses associated with severe illness in humans. Some were identified for the first time in the Arabian Received: 15 June 2021 Peninsula. The human disease-associated viruses detected included Crimean Congo Hemorrhagic Accepted: 15 July 2021 fever virus and Tamdy virus (family Nairoviridae), Guertu virus (family Phenuiviridae), and a novel Published: 18 July 2021 coltivirus that shares similarities with Tarumizu virus, Tai forest reovirus and Kundal virus (family Reoviridae). Furthermore, Alkhurma hemorrhagic virus (Flaviviridae) was detected in two tick Publisher’s Note: MDPI stays neutral pools by specific qPCR. In addition, tick-specific viruses in families Phenuiviridae (phleboviruses), with regard to jurisdictional claims in Iflaviridae, Chuviridae, Totiviridae and Flaviviridae (Pestivirus) were detected. The presence of published maps and institutional affil- human pathogenetic viruses warrants further efforts in tick surveillance, xenosurveillence, vector iations. control, and sero-epidemiological investigations in human and animal populations to predict, contain and mitigate future outbreaks in the region. Keywords: virome analysis; Hyalomma dromedarii; dromedary camels; province of Makkah; Saudi Copyright: © 2021 by the authors. Arabia; arboviruses; tick-borne diseases Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons 1. Introduction Attribution (CC BY) license (https:// Recently, Saudi Arabia has witnessed an upsurge of viruses with high morbidity and creativecommons.org/licenses/by/ mortality rates in humans and livestock. Some of these, e.g., the Middle East Respiratory 4.0/). Viruses 2021, 13, 1396. https://doi.org/10.3390/v13071396 https://www.mdpi.com/journal/viruses Viruses 2021, 13, 1396 2 of 13 Syndrome (MERS) virus and Alkhurma hemorrhagic fever virus (AHFV), emerged for the first time, while others, e.g., dengue virus, Crimean-Congo hemorrhagic fever virus (CCHFV), Kadam virus (KADV), West Nile virus, Rift Valley fever virus and chikungunya virus, have re-emerged after spreading in other parts of the world [1–3]. Most emerging human viral diseases are of zoonotic origin, and 40% of these are vector- dependent [4]. Ticks are hematophagous vectors capable of transmitting viruses to human and animal hosts. Several studies have found pathogenic viruses from different species of ticks in Saudi Arabia. For instance, CCHFV was isolated from Hyalomma, Rhipicephalus and Amblyomma ticks infesting small ruminants imported from Sudan to Saudi Arabia in 2000 [5]. In 2007, AHFV RNA was detected in Ornithodoros savignyi ticks from the Western part of Saudi Arabia after several human cases were reported [6]. Another study confirmed the circulation of the AHFV in O. savignyi and H. dromedarii ticks in the Najran region (southwestern part) of the kingdom [7]. Sindbis virus (SINV) was isolated from Hyalomma species (H. dromedarii and H. impeltatum) in the Al-Qassim, Riyadh and Jazan regions [8]. Dhori virus was also isolated and identified (H. impeltatum and H. schulzei) in the eastern region [8]. In the early 1980s, KADV (Flavivirus) was detected in a pool of male H. dromedarii ticks taken from a dead camel in Wadi Thamamah in Riyadh [3]. Before that, KADV was isolated from Rhipicephalus and Amblyomma ticks in Uganda and Kenya and was serologically associated with human and cattle infection. Another study confirmed the isolation of KADV from H. dromedarii and H. anatolicum in the Al-Qassim region of Saudi Arabia [8]. Hyalomma ticks are common in the Arabian Peninsula and other Asian countries [9,10]. They belong to the family of hard ticks Ixodidae and ectoparasitize camels. Dromedary or Arabian camels are the main domesticated animals in Saudi Arabia and are of economic and medical importance. Recently, camels have been associated with the transmission of several viral diseases to humans. KADV, AHFV, CCHFV, Tamdy virus (TOV) and MERS are associated with camels [3,11–13]. For instance, Hemida et al. found that 90% of camel populations were MERS-CoV seropositive [13]. Recently, a novel lineage of CCHFV has been identified in the nasopharyngeal samples collected from camels in the United Arab Emirates [11]. Dromedary camels are also associated with prions and severe forms of neurodegenerative prion disease [14] as well as several bacterial pathogens [9]. In this study, we identified viral pathogens from ticks infesting dromedary camels in the Makkah province of Saudi Arabia using a metagenomic approach [15]. Earlier studies have shown that metagenomic approaches can be used to detect both known and novel viruses associated with animal and human diseases [16,17]. Such approaches can enable timely responses to vector-borne disease outbreaks and help in preparedness as well as the implementation of practical strategies and policies to contain and mitigate the threat of these infections. 2. Research Methodology 2.1. Makkah Region The Makkah (Mecca) region is located on the western Arabian Peninsula. It includes important cities such as Makkah (Mecca), the holiest city in the Islamic world, Jeddah, the biggest sea port on the Red Sea and Al-Taif, with a population of 8.8 million (Figure1 ). Millions of Muslim pilgrims gather and slaughter more than 1.2 million sheep, goats and camels annually during their pilgrimage [18], as a part of their religious rituals. This may enhance the transmission of infectious diseases, including zoonotic and vector-borne diseases. The climate of Makkah is arid, and most animals that live in the region are adapted to this aridity. Viruses 2021,, 13,, 1396x FOR PEER REVIEW 3 of 13 Figure 1. A map of the western part of Saudi Arabia showing the mainmain identifiedidentified potential path pathogensogens in the province of Makkah. 2.2.2.2. Tick Tick Collection FromFrom the mid-Julymid-July toto OctoberOctober 2019, 2019, a a total total of of 200 200 camels camels were were screened screened for for ticks ticks in the in ◦ 0 00 ◦ 0 00 thewestern western part part of Saudiof Saudi Arabia, Arabia, Al-Taif Al-Taif (Coordinates: (Coordinates: 21 21°1616 30.34′30.34″N N 40 40°2424 22.16′22.16″ E) and ◦ 0 ◦ 0 Al-Khurma (21°55 (21 55′ NN 42°02 42 02′ E)E) (Figure (Figure 11).). Each camel waswas apparentlyapparently healthyhealthy atat thethe timetime ofof sampling. Ticks Ticks found within 15 min were collected (1 tick per infested animal), and a totaltotal of of 200 200 ticks ticks (100 (100 ticks ticks from from each each locality) locality) were were collected collected and and placed placed in in separate separate tubes, tubes, containingcontaining RNAlater. TheThe samplessamples were were shipped shipped to to the the University University of Helsinki,of Helsinki, Finland, Finland, for forfurther further analysis. analysis. 2.3. Tick Species Identification 2.3. Tick Species Identification Ticks were morphologically identified to genus level. Two legs from each tick were Ticks were morphologically identified to genus level. Two legs from each tick were separated for DNA extraction and barcode sequencing. DNA was extracted using GeneJET separated for DNA extraction and barcode sequencing. DNA was extracted using Genomic DNA purification kit (Thermo Scientific). A 604 bp fragment of the cytochrome c GeneJET Genomic DNA purification kit (Thermo Scientific). A 604 bp fragment of the cy- oxidase subunit 1 (cox1) gene was amplified as described previously [19,20]. The Phusion tochrome c oxidase subunit 1 (cox1) gene was amplified as described previously [19,20].
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