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Novel Coronaviruses, Astroviruses, Adenoviruses and Circoviruses in Insectivorous Bats from Northern China

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Novel Coronaviruses, Astroviruses, Adenoviruses and Circoviruses in Insectivorous Bats from Northern China Received: 17 November 2016 DOI: 10.1111/zph.12358 ORIGINAL ARTICLE Novel coronaviruses, astroviruses, adenoviruses and circoviruses in insectivorous bats from northern China H.-J. Han1 | H.-L. Wen1 | L. Zhao1 | J.-W. Liu1 | L.-M. Luo2 | C.-M. Zhou1 | X.-R. Qin1 | Y.-L. Zhu1 | M.-M. Liu1 | R. Qi1 | W.-Q. Li1 | H. Yu3 | X.-J. Yu4,5 1School of Public Health, Shandong University, Jinan, Shandong, China Summary 2Shandong Center for Disease Control and Bats are considered as the reservoirs of several emerging infectious disease, and novel Prevention, Jinan, Shandong, China viruses are continually found in bats all around the world. Studies conducted in southern 3Schools of Medicine, Fudan University, China found that bats carried a variety of viruses. However, few studies have been con- Shanghai, China 4Wuhan University School of Health Sciences, ducted on bats in northern China, which harbours a diversity of endemic insectivorous Wuhan, Hubei, China bats. It is important to understand the prevalence and diversity of viruses circulating in 5 Departments of Pathology and Microbiology bats in northern China. In this study, a total of 145 insectivorous bats representing six and Immunology, University of Texas Medical Branch, Galveston, TX, USA species were collected from northern China and screened with degenerate primers for viruses belonging to six families, including coronaviruses, astroviruses, hantaviruses, par- Correspondence Xue-Jie Yu, University of Texas Medical amyxoviruses, adenoviruses and circoviruses. Our study found that four of the viruses Branch, Galveston, TX, USA. screened for were positive and the overall detection rates for astroviruses, coronaviruses, Email: [email protected] adenoviruses and circoviruses in bats were 21.4%, 15.9%, 20% and 37.2%, respectively. Funding information In addition, we found that bats in northern China harboured a diversity of novel viruses. The Shandong Province Science and Technology Development Program, Grant/ Common Serotine (Eptesicus serotinu), Fringed long- footed Myotis (Myotis fimriatus) and Award Number: 2014GSF121004; The Peking Myotis (Myotis pequinius) were investigated in China for the first time. Our study National Natural Science Funds of China, Grant/Award Number: 31570167, 81102171 provided new information on the ecology and phylogeny of bat- borne viruses. and 31402173 KEYWORDS adenoviruses, astroviruses, bats, China, circoviruses, coronaviruses 2012; Xu et al., 2015; Yang et al., 2013; Yuan et al., 2014). However, so 1 | INTRODUCTION far, few studies have been conducted on bats in northern China, which harbours a diversity of endemic insectivorous bats. To ascertain the The majority of emerging infectious diseases (EIDs) of humans are prevalence and diversity of viruses circulating in bats in northern China, zoonoses originating from wildlife (Lloyd- Smith et al., 2009; Wolfe, insectivorous bat representing six species were collected and screened Dunavan, & Diamond, 2007). As the second largest order of mammals, for viruses belonging to six families including coronaviruses, astroviruses, bats are considered as the reservoirs of several emerging infectious hantaviruses, paramyxoviruses, adenoviruses and circoviruses. disease, such as Ebola, Marburg, SARS, MERS and Henipavirus disease (Han et al., 2015). 2 | MATERIALS AND METHODS Since the outbreak of SARS in 2003, interest in bat- borne viruses has been increasing and novel viruses are continually found in bats all around 2.1 | Sample collection the world. A number of studies reported that bats, especially from south- ern China, carried a variety of viruses (Chu, Poon, Guan, & Peiris, 2008; Bats were collected in various habitats, including karst caves, city Ge et al., 2011, 2012, 2016; Hu et al., 2014; Li et al., 2010; Wu et al., sewers and human houses in Mengyin County, Shandong Province This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2017 The Authors. Zoonoses and Public Health Published by Blackwell Verlag GmbH. 1 |  wileyonlinelibrary.com/journal/zph Zoonoses Public Health. 2017;1–11. 2 | HAN ET AL. of China, from March to October, 2015. Bat species was molecularly identified by amplification and sequencing of the cytochrome B (cytB) Impacts gene with bat liver DNA as described previously (Ishii et al., 2014; • We conducted a survey of viruses in bats in northern Linacre & Lee, 2005). Captured bats were euthanized by intramus- China; a total of 145 insectivorous bats representing six cular injection of overdose chloral hydrate. Thoracic and abdominal species were screened with degenerate primers for organs were collected and stored at −80°C until analysis. viruses belonging to six families, including coronaviruses, This study was carried out in accordance with the Guidelines of astroviruses, hantaviruses, paramyxoviruses, adenovi- Regulations for the Administration of Laboratory Animals (Decree No. ruses and circoviruses. 2 of the State Science and Technology Commission of the People’s • Bats in northern China harboured a diversity of novel vi- Republic of China, 1988). The collection of bats for this study was ap- ruses that might be of public health significance. proved by the Ethics Committee of Prevention Medicine of Shandong • To our knowledge, this represented the first documenta- University (No. 20150501), and all efforts were made to minimize dis- tions of viruses in Common Serotine (Eptesicus serotinu), comfort to animals. Fringed long-footed Myotis (Myotis fimriatus) and Peking Myotis (Myotis pequinius) in China. 2.2 | Preparation of samples and PCR screening for viruses RNA and DNA were extracted separately from intestinal and 2.3 | Phylogenetic analysis spleen samples using AllPrep DNA/RNA Mini Kit (Qiagen, Hilden, Germany), and RNA was extracted from kidney and lung tissue Sequence chromatograms and sequence analysis were examined with RNeasy Mini Kit (Qiagen) according to the manufacturer’s in- with Chromas 2.6 (http://technelysium.com.au/wp/chromas) and structions. PCR screening for viruses was performed using broadly BLAST program (http://blast.ncbi.nlm.nih.gov/Blast.cgi), respectively. reactive consensus PCR assays targeting RNA viruses including Sequences were aligned and trimmed with MEGA 7.0. Phylogenetic coronaviruses (Woo et al., 2005), astroviruses (Chu et al., 2008), trees were constructed with MEGA 7.0 (www.megasoftware.net) by hantaviruses (Klempa et al., 2006), paramyxoviruses (Tong, Chern, using the neighbour- joining method with an amino acid percentage Li, Pallansch, & Anderson, 2008), DNA viruses including adenovi- distance substitution model and complete deletion option, and boot- ruses (Wellehan et al., 2004) and circoviruses (Lima et al., 2015). strap values were calculated with 1,000 replicates. Paramyxoviruses were screened with one- step RT- PCR with Access RT- PCR System (Promega, Madison, WI), while screening for coro- 3 | RESULTS naviruses, astroviruses and hantaviruses, cDNA was first generated by using reverse transcription system (Promega) with random prim- 3.1 | Molecular detection of viruses in bats ers. Detailed information of primer sequences and amplicon lengths is listed in Table S1. A total of 145 insectivorous bats were collected for microbiological PCR products were analyzed using 1.2% agarose gel electrophore- studies from Mengyin County of Shandong Province, China. They sis and detected with ethidium bromide staining under UV light. PCR were molecularly identified into six species, with four from the family products of expected size were excised from gels and extracted with Vespertilionidae and two from the family Rhinolophidae (Table 1). The Gel Extraction Kit (Promega) and were then cloned into pMD 19- T partial cytB gene for the six bat species was deposited in GenBank with vectors (TaKaRa, Shiga, Japan) for sequencing. Three recombined plas- accession numbers KX655809, KX655810, KX655817, KX655826, mids for each PCR product were sequenced on both strands. KX655831, KX655837 and KX655840. TABLE 1 Prevalence of viruses in bats from northern China Family Species Common name No. sampled AstVs CoVs PMVs HTVs AdVs CVs Vespertilionidae Eptesicus serotinus Common Serotine 26 8 11 0 0 2 1 Myotis fimbriatus Fringed long- footed Myotis 34 14 6 0 0 18 29 Myotis ricketti Rickett’s big- footed Myotis 10 1 2 0 0 5 6 Myotis pequinius Peking Myotis 57 8 3 0 0 4 15 Rhinolophidae Rhinolophus ferrumequinum Greater Horseshoe Bat 4 0 0 0 0 0 1 Rhinolophus pusillus Least Horseshoe Bat 14 0 1 0 0 0 2 145 31 22 0 0 29 51 AstVs, astroviruses; CoVs, coronaviruses; PMVs, paramyxoviruses; HTVs, hantaviruses; AdVs, adenoviruses; CVs, circoviruses. HAN ET AL. | 3 None of the bats screened were positive for hantaviruses or may represent a novel coronavirus. Significantly, genotype I and II in paramyxoviruses, despite previous studies reporting their existence the β- CoV genus clustered with lineage C β- CoV and shared 85%–88% in bats. The overall detection rates for astroviruses, coronaviruses, nucleotide identity with MERS- CoV, which was the causative agent adenoviruses and circoviruses in bats were 21.4% (31/145), 15.9% of the Middle East Respiratory Diseases (MERS). Partial pol gene se- (23/145), 20% (29/145) and 37.2% (54/145), respectively. Four spe- quences of bat coronaviruses of this study were deposited in GenBank cies from the family Vespertilionidae were all positive for astroviruses, with accession numbers KY009612–KY009634.
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