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(Chiroptera: Vespertilionidae) and the Bat Soft Tick Argas Vespe

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(Chiroptera: Vespertilionidae) and the Bat Soft Tick Argas Vespe Zhao et al. Parasites Vectors (2020) 13:10 https://doi.org/10.1186/s13071-020-3885-x Parasites & Vectors SHORT REPORT Open Access Rickettsiae in the common pipistrelle Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) and the bat soft tick Argas vespertilionis (Ixodida: Argasidae) Shuo Zhao1†, Meihua Yang2†, Gang Liu1†, Sándor Hornok3, Shanshan Zhao1, Chunli Sang1, Wenbo Tan1 and Yuanzhi Wang1* Abstract Background: Increasing molecular evidence supports that bats and/or their ectoparasites may harbor vector-borne bacteria, such as bartonellae and borreliae. However, the simultaneous occurrence of rickettsiae in bats and bat ticks has been poorly studied. Methods: In this study, 54 bat carcasses and their infesting soft ticks (n 67) were collected in Shihezi City, north- western China. The heart, liver, spleen, lung, kidney, small intestine and large= intestine of bats were dissected, followed by DNA extraction. Soft ticks were identifed both morphologically and molecularly. All samples were examined for the presence of rickettsiae by amplifying four genetic markers (17-kDa, gltA, ompA and ompB). Results: All bats were identifed as Pipistrellus pipistrellus, and their ticks as Argas vespertilionis. Molecular analyses showed that DNA of Rickettsia parkeri, R. lusitaniae, R. slovaca and R. raoultii was present in bat organs/tissues. In addition, nine of the 67 bat soft ticks (13.43%) were positive for R. raoultii (n 5) and R. rickettsii (n 4). In the phylo- genetic analysis, these bat-associated rickettsiae clustered together with conspecifc= sequences reported= from other host and tick species, confrming the above results. Conclusions: To the best of our knowledge, DNA of R. parkeri, R. slovaca and R. raoultii was detected for the frst time in bat organs/tissues. This is also the frst molecular evidence for the presence of R. raoultii and R. rickettsii in bat ticks. To our knowledge, R. parkeri was not known to occur in Asia. Our results highlight the need to assess rickettsial agents in a broader range of bat species and associated tick species. Keywords: Rickettsia, Chiroptera, Vespertilionidae, Argasidae Background widespread distribution and may even undergo short- Bats (order Chiroptera), including at least 1400 species to long-distance seasonal migration [2]. Bats are special [1], are the only mammals which actively fy [2]. Among in their capacity to act as reservoir hosts for intracellu- the consequences of this trait, bats show a geographically lar pathogens [3]. Several species of bat-associated soft (Acari: Argasidae) and hard (Acari: Ixodidae) ticks, i.e. Carios kelleyi, Argas vespertilionis, A. transgariepinus, *Correspondence: [email protected] Ornithodoros sp., Ixodes vespertilionis, I. ariadnae and I. †Shuo Zhao, Meihua Yang and Gang Liu contributed equally to this work 1 School of Medicine, Shihezi University, Shihezi 832002, Xinjiang Uygur simplex, were shown to carry DNA of vector-borne bac- Autonomous Region, People’s Republic of China teria and protozoans [4, 5]. Among these tick species, A. Full list of author information is available at the end of the article vespertilionis (which has a wide distribution in Europe, © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea- tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo- main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhao et al. Parasites Vectors (2020) 13:10 Page 2 of 6 Africa and Asia) was reported to bite humans [6]. In addi- Detection of rickettsiae, sequencing and phylogenetic tion, increasing molecular evidence supports that bats analyses and/or their ticks may harbor vector-borne zoonotic bac- Four genetic markers, including 17 kDa antigen (17-kDa), teria, such as bartonellae and borreliae [7, 8]. However, citrate synthase (gltA), and outer membrane proteins A the occurrence of rickettsiae in bats and bat ticks appears and B (ompA and ompB) genes were assessed within each to be poorly studied, particularly in Eurasia. sample to investigate the presence of rickettsiae [15]. Rickettsiae are Gram-negative, obligatory intracel- Te primers and PCR cycling conditions in this study lular bacteria, which may cause disease in animals and are shown in Additional fle 1: Text S1 and Table S1. humans, and are associated with arthropod vectors (such Each PCR assay included a negative control (distilled as ticks, lice, feas or mites), both as transmitters and res- water instead of tick DNA template) and a positive con- ervoirs [9]. Concerning rare reports on rickettsiae from trol (containing sequence-verifed DNA from R. raoultii bats and their ticks, previously Rickettsia africae was obtained from the tick Dermacentor nuttalli collected detected in the blood of bats in the Caribbean region [10] in XUAR) [15]. Purifcation and sequencing of the PCR and several rickettsiae were identifed in bat ticks from products were performed as described above [16, 17]. Central America, Europe, Africa and Asia [11]. However, Sequences were manually edited, aligned and com- to the best of our knowledge, a simultaneous analysis of pared to reference GenBank sequences by nucleotide bat tissues and bat ticks for the presence of rickettsiae BLASTn program (https ://blast .ncbi.nlm.nih.gov). A in central Asia has not been carried out. Our hypothesis phylogenetic tree was constructed using the maximum- is that bats might be susceptible to infection with some likelihood and neighbor-joining algorithms implemented rickettsial species. In our study, we aimed at evaluating in MEGA 6.0 software [18]. the susceptibility of bats to rickettsial infection and the involvement of these fying mammals and their ticks in Results Rickettsia transmission cycles in central Asia. All bats were identifed as Pipistrellus pipistrellus, and their ticks as A. vespertilionis. Out of 378 bat organs/tis- Methods sues and 67 bat ticks, 6 bats and 9 ticks were positive for Sample collection and identifcation the four Rickettsia genetic markers (17-kDa, gltA, ompA Fifty-four bat carcasses were collected from an idle class- and ompB). Sequencing identifed R. parkeri in the heart, room in Shihezi University, Xinjiang Uygur Autonomous liver and kidney of a bat, R. lusitaniae in the heart, liver Region (XUAR) in northeastern China during 2015– and small intestine of a bat, R. slovaca in the lung and 2019. Te heart, liver, spleen, lung, kidney, small intes- kidney of two bats and R. raoultii was only found in the tine and large intestine of bat carcasses were removed, liver of two bats (Fig. 1, Table 1). Concerning bat ticks, R. similarly to what has been reported in studies of bat raoultii was detected in fve and R. rickettsii in four speci- haemoparasites [12]. Genomic DNA was extracted from mens. Interestingly, four ticks positive to R. raoultii were these organs, as well as from ticks collected from the removed from a R. raoultii-positive bat. bats using the 96 Flux Automatic Nucleic Acid Extrac- Regarding sequence comparisons based on the four tion Instrument (Bio Teke, Beijing, People’s Republic of genetic markers, R. parkeri in this study had sequence China) with a matching commercial kit (Cell & Tissue identities within the range of 99.7–100% when compared Kit, Bio Teke) according to the manufacturer’s instruc- with the sequence of R. parkeri from the tick Ambly- tions. To confrm the morphological identifcation of omma ovale in Colombia (GenBank: CP040325); Rick- bats, the cytochrome b (cytb) gene was analyzed [13] and ettsia lusitaniae showed 98.6–100% identity compared a representative cytb sequence was deposited in the Gen- with the sequence of R. lusitaniae from A. vespertilionis Bank database under the accession number MF106222. infesting P. pipistrellus in China [11]; Rickettsia slovaca Simultaneously, a total of 67 tick larvae were collected had 99.8% sequence identity with a conspecifc bacte- from bat bodies. Te ticks were morphologically identi- ria from Dermacentor marginatus in Turkey; Rickettsia fed according to the standard taxonomic keys as previ- raoultii showed 99.1–100% identity with R. raoultii from ously described [14]. From fve ticks, the 16S rDNA gene D. nuttalli infesting Spermophilus undulatus in north- was amplifed following a previously reported protocol western China [13]; and Rickettsia rickettsii was 99.7– [15]. Te corresponding 16S rDNA sequence was depos- 99.9% identical to R. rickettsii from D. variabilis in the ited in the GenBank database under the accession num- USA [19]. Te detailed similarities and divergences of the ber MF106219. sequences in this study are shown in Table 2 and Addi- tional fle 2: Table S2. Zhao et al. Parasites Vectors (2020) 13:10 Page 3 of 6 Fig. 1 Phylogenetic tree of the ompA-gltA-ompB concatenated sequences for the rickettsial agents in bats and their infesting ticks. The new sequences provided by the present study are indicated by a black triangle Table 1 The prevalence of Rickettsia parkeri, R. lusitaniae, R. slovaca, R. raoultii, R. rickettsii detected in the bat organs Species Heart Liver Spleen Lung Kidney Small intestine Large intestine R. parkeri 1/54 (1.9%) 1/54 (1.9%) – – 1/54 (1.9%) – – R.
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