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Anaplasma Platys Guo et al. BMC Infectious Diseases (2019) 19:434 https://doi.org/10.1186/s12879-019-4075-3 RESEARCH ARTICLE Open Access Molecular identification and characterization of Anaplasma capra and Anaplasma platys-like in Rhipicephalus microplus in Ankang, Northwest China Wen-Ping Guo1,2*† ,BingZhang3†, Yi-Han Wang1,2,GangXu1,2,XiaoquanWang4,XuebingNi5 and En-Min Zhou1,2 Abstract Background: Four species within Anaplasma genus are emerging zoonotic pathogens, which are transmitted by ticks and generate veterinary and public health concerns. Here, we performed a molecular survey of Anaplasma in Ankang, Northwest China. Methods: Hard ticks were collected and identified using morphological and molecular methods. Human-pathogenic Anaplasma species were tested using nested polymerase chain reaction. The nearly complete rrs, gltA,andgroEL genes sequences from revealed Anaplasma species were amplified and sequenced to determine their molecular characteristics and their phylogeny. Results: All ticks collected in Ankang belonged to the Rhipicephalus microplus. Novel unclassified Anaplasma strains genetically related to A. platys and A. capra were detected in these ticks. Co-infection of these two organisms was also found. The novel unclassified Anaplasma strains identified in this study formed a distinct phylogenetic lineage based on the groEL gene and two lineages based on the gltA gene within A. platys and related strains group. The revealed A. capra strains identified in this study were most closely related to those detected in humans and other vertebrate animals. Conclusion: We revealed the presence of A. capra, a novel human pathogens in R. microplus ticks in previously unrecognized endemic regions. We also detected a novel unclassified Anaplasma species genetically related to A. platys. The epidemiology of anaplasmosis caused by these two Anaplasma species in humans should be assessed in future studies. Keywords: Anaplasma capra, Anaplasma platys-like strains, China, Rhipicephalus microplus ticks, Rrs, gltA,AndgroEL genes Background livestock have received increasing attention since the first Anaplasma genus comprises a group of Gram-negative incidence of human granulocytic anaplasmosis (HGA) obligate intracellular bacteria that inhabit diverse eukaryotic caused by A. phagocytophilum was reported [4]. During this hosts. Seven classified species have been described in this period, many known and emerging Anaplasma species genus so far [1–3]. In the last two decades, the rapidly have been proved to be pathogenic to humans, causing ana- spreading diseases caused by Anaplasma in humans and plasmosis or associated diseases. For instance, A. ovis and A. platys have been identified as human pathogens [5, 6], and A. capra,anovelAnaplasma species, was also con- * Correspondence: [email protected] †Wen-Ping Guo and Bing Zhang contributed equally to this work. firmed to be a human pathogen in China [3]. Among these 1Department of Preventive Veterinary Medicine, College of Veterinary causative agents, A. phagocytophilum is the most Medicine, Northwest A&F University, Xinong Road 22, Yangling 712100, common pathogen with a worldwide distribution [1, 7], Shaanxi, China 2Scientific Observing and Experimental Station of Veterinary Pharmacology while others are usually neglected because the cases and Diagnostic Technology, Ministry of Agriculture, Yangling, Shaanxi, China occur only sporadically. Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Guo et al. BMC Infectious Diseases (2019) 19:434 Page 2 of 9 Since 1982, several classified species and unclassified ticks from domestic animals in Ankang city and screened strains belonging to Anaplasma genus have been re- them for Anaplasma spp. ported in ticks and mammals from China [3, 8, 9]. Human-pathogenic species and unclassified strains within Methods Anaplasma have been identified, including A. capra, A. Collection of tick samples ovis, A. phagocytophlum,andA. platys. To date, only HGA Ankang city is located in Northwest China, southeast caused by A. phagocytophilum has been reported [10]. In of Shaanxi Province and south of the Qinling contrast, less attention has been paid to the epidemiology Mountains (31°42′ to 33°50′N, 108°00′ to 110°12′E). and genetic characteristics of other pathogens, although Its topography is characterized by densely vegetated they have been reported in ticks and livestock. In North- mountains and hills, and livestock often become west China, molecular epidemiological surveys confirmed heavily infested with ticks when they graze in the thepresenceofthefourAnaplasma species mentioned field. In this study, ticks were sampled in 2017 and above: A. phagocytophilum and A. ovis in Qinghai Province; 2018 from the body surface of cattle, goats, or A. ovis in Tibet [11]; A. platys, A. ovis,andA. capra in sheep, and one tick per animal was collected from Gansu Province [12–14]; and A. platys and A. ovis in seven sampling sites (Fig. 1). These animal hosts of Xinjiang Uygur Autonomous Region [15–17]. ticks were privatedly-owned and verbal consent was Shaanxi Province is located in Northwest China, form- obtained from the owners of these animals for tick ing a gateway to four other provinces in this region and samples to be taken. The ticks were first identified connecting the East, Central, and Northwest China. Previ- by morphology [19, 20], and the identification of ous studies have revealed the presence of at least 26 tick one-quarter of adults and all nymphs was further speciesinthisregion[18], but none of them has attempted confirmed by analyzing 710-bp of the COI gene to molecularly characterize the human-pathogenic Ana- using the LCO1490 and HCO2198 primers [21]. The plasma species that they may host. To know more about Institutional Animal Care and Use Committee of the circulation and the genetic characteristic of human- Northwest A&F University have reviewed and ap- pathogenic Anaplasma species in Shaanxi, we sampled proved this study. Fig. 1 Map with the coordinates of all seven sampling sites (★) in Ankang, Shaanxi Province, China. The maps of Ankang city and Shaanxi Province was generated using ArcGIS (version 10.0; http://www.arcgis.com/index.html) and edited using Adobe Illustrator. The map of China was obtained from http://english.freemap.jp/item/asia/china.html Guo et al. BMC Infectious Diseases (2019) 19:434 Page 3 of 9 DNA extraction and detection of Anaplasma species For A. capra, the former fragment was amplified with The total DNA was extracted from the whole body of each fD1/Ehr2 primer pairs for the primary round and fD1/ tick. The ticks were first washed with 75% alcohol and Ehr4 for the secondary round of semi-nested PCR, and then with phosphate-buffered saline. After washing, the the latter fragment was amplified with Ehr1/rp2 for the total DNA was extracted from individual ticks using Tis- primary round and Ehr3/rp2 for the secondary round of sue DNA Kit (Omega, Norcross, GA, USA) according to semi-nested PCR [25, 28]. The same strategy was used the manufacturer’s instructions. The DNA samples were to amplify the almost full-length rrs gene of A. platys diluted in 80 μL of the elution buffer and stored at − 20 °C. and related strains, and only the primer PLATYS primer The extracted DNA samples were initially screened for was used instead of fD1. the presence of Anaplasma spp. by amplifying the rrs The partial gltA gene of A. platys and related strains gene using nested polymerase chain reaction (PCR) with was amplified with Pglt-F/Pglt-R1 primers for the pri- primers specific for A. phagocytophilum, A. ovis, and A. mary round and Pglt-F/Pglt-R2 for the secondary round capra as described previously [22–26]. The primers of semi-nested PCR. The partial groEL gene were ampli- PLATYS [27], Ehr2, and Ehr4 [28] were used to detect fied with Pgro-F1/Pgro-R primers for the primary round A. platys by semi-nested PCR, also targeting the rrs and Pgro-F2/Pgro-R for the secondary round of semi- gene. The primer sequences are shown in the Table 1. nested PCR (Additional file 1: Figure S1). Double-distilled water was used as a negative control, The nearly complete groEL and gltA genes of A. and the extracted DNA samples positive for these four capra were obtained according to Guo et al. [29]. By Anaplasma species were used as positive controls. To amplifying two overlapping fragments, almost-full-length avoid contamination, the DNA extraction, PCR mixture groEL and gltA genes of A. platys and related strains were preparation, template addition, and agarose gel electro- amplified using semi-nested PCR (Additional file 1:Figure phoresis were performed in a fume hood in four separate S1). The former fragment of gltA was amplified with rooms and filter tips were used in these processes. Pglt-F/Pglt-R1 primer pairs for the primary round and Pglt-F/Pglt-R2 for the secondary round of semi-nested Amplification of nearly complete rrs, and partial/nearly PCR,whereasthelatterfragmentofgltA was amplified with complete groEL and gltA genes Pglt-L-F1/Pglt-L-R for the primary round and Pglt-L-F2/ The positive samples were used to amplify the nearly Pglt-L-R for the secondary round. For the nearly complete complete rrs gene, and the molecular characteristics of groEL gene, the former fragment was amplified with the revealed Anaplasma strains were analyzed using par- Pgro-F-F/Pgro-F-R1 for the primary round and Pgro-F-F/ tial and/or nearly complete groEL and gltA genes.
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