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Discovery of a Highly Divergent Hepadnavirus in Shrews from China

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Discovery of a Highly Divergent Hepadnavirus in Shrews from China Virology 531 (2019) 162–170 Contents lists available at ScienceDirect Virology journal homepage: www.elsevier.com/locate/virology Discovery of a highly divergent hepadnavirus in shrews from China T Fang-Yuan Niea,b,1, Jun-Hua Tianc,1, Xian-Dan Lind,1, Bin Yuc, Jian-Guang Xinge, Jian-Hai Caof, ⁎ ⁎⁎ Edward C. Holmesg,h, Runlin Z. Maa, , Yong-Zhen Zhangb,h, a State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China b State Key Laboratory for Infectious Disease Prevention and Control; Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases; Department of Zoonoses, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Changping, Beijing, China c Wuhan Center for Disease Control and Prevention, Wuhan, China d Wenzhou Center for Disease Control and Prevention, Wenzhou, Zhejiang Province, China e Wencheng Center for Disease Control and Prevention, Wencheng, Zhejiang Province, China f Longwan Center for Disease Control and Prevention, Longwan District, Wenzhou, Zhejiang Province, China g Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2006, Australia h Shanghai Public Health Clinical Center & Institute of Biomedical Sciences, Fudan University, Shanghai, China ARTICLE INFO ABSTRACT Keywords: Limited sampling means that relatively little is known about the diversity and evolutionary history of mam- Hepadnaviruses malian members of the Hepadnaviridae (genus Orthohepadnavirus). An important case in point are shrews, the Shrews fourth largest group of mammals, but for which there is limited knowledge on the role they play in viral evo- Phylogeny lution and emergence. Here, we report the discovery of a novel shrew hepadnavirus. The newly discovered virus, Evolution denoted shrew hepatitis B virus (SHBV), is divergent to be considered a new species of Orthohepadnavirus. Cross-species transmission Phylogenetic analysis revealed that these viruses were usually most closely related to TBHBV (tent-making bat hepatitis B virus), known to be able to infect human hepatocytes, and had a similar genome structure, although SHBV fell in a more basal position in the surface protein phylogeny. In sum, these data suggest that shrews are natural hosts for hepadnaviruses and may have played an important role in their long-term evolution. 1. Introduction nackednaviruses, were discovered in fish (Lauber et al., 2017). Despite their diversity, all members of the mammalian genus Orthohepadnavirus Hepadnaviruses (family Hepadnaviridae) are characterized by par- contain four overlapped open reading frames (ORFs): polymerase (P), tially circular, double-stranded DNA genomes (~3.2 kb in length). core protein (C), surface protein (S) and X protein. The large S mRNA is Interestingly, the replication of these viruses requires an RNA inter- thought to encode three proteins - the preS1, preS2 and S. The preS1 is mediate produced by reverse transcription (Urban et al., 2010). At a domain involved in virus-host interaction via cell receptors (Neurath present, the Hepadnaviridae are classified into three genera: Avihe- et al., 1986). padnavirus, Orthohepdnavirus and one unassigned genus (https://talk. HBV is an important and globally distributed viral pathogen af- ictvonline.org/taxonomy/). As their names imply, avihepadnaviruses fecting approximately 257 million people worldwide and causing have been identified in birds (e.g. ducks and parrots) while orthohe- around 887,000 deaths annually, mostly as a consequence of cirrhosis padnaviruses are associated with mammals, including human hepatitis and hepatocellular carcinoma (http://www.who.int/en/news-room/ B virus (HBV). The unassigned genus contains two hepadnavirus species fact-sheets/detail/hepatitis-b). While the majority of human patho- found in fish - white sucker hepatitis B virus and bluegill hepatitis B gens causing emerging infectious diseases have an animal origin (Wolfe virus - and a single virus associated with the Tibetan frog (Tibetan frog et al., 2007), the host range of the known orthohepadnavirus is limited hepatitis B virus). Recently, highly divergent non-enveloped viruses and the evolutionary history of orthohepadnavirus is therefore unclear. that are the sister-group to the hepadnaviruses, denoted the Although rodents comprise approximately 42% of living mammalian ⁎ Corresponding author. ⁎⁎ Correspondence to: State Key Laboratory for Infectious Disease Prevention and Control, National Institute of Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Changping Liuzi 5, Beijing 102206, China. E-mail addresses: [email protected] (R.Z. Ma), [email protected] (Y.-Z. Zhang). 1 Contributed to this work equally. https://doi.org/10.1016/j.virol.2019.03.007 Received 23 January 2019; Received in revised form 7 March 2019; Accepted 8 March 2019 Available online 11 March 2019 0042-6822/ © 2019 Elsevier Inc. All rights reserved. F.-Y. Nie, et al. Virology 531 (2019) 162–170 species (Wilson and Reeder, 2005), to date only ground squirrels (genus Wufeng-As-178, Wufeng-As-205) based on host species and sampling Marmota) appear to be natural rodent hosts of the virus (Summers et al., sites (Table 1). 1978; Marion et al., 1980; Testut et al., 1996). Similarly, bats comprise Notably, no hepadnavirus was detected in Suncus murinus (Asian around 20% of living mammalian species and are also natural he- house shrews), although 170 of these animals were captured and padnavirus reservoirs (He et al., 2013, 2015; Drexler et al., 2013; Wang screened (Table 1). Moreover, other rodent species from the same dis- et al., 2017a; Nie et al., 2018). Although a divergent orthohepadnavirus trict captured during the same years and from the same geographic was recently identified in domestic cats (cat hepadnavirus, CHV) were also screened for hepadnaviruses, but none were positive (data not (Aghazadeh et al., 2018), the only other mammalian species that ap- shown). Clearly, however, larger-scale sampling is needed to accurately pear to be natural hosts of orthohepadnavirus are primates, including document the prevalence of hepadnaviruses in shrews and rodents. divergent viruses present in the woolly monkey (WMHBV) (Lanford et al., 1998; Rasche et al., 2016) and capuchin monkey (CMHBV) (de 2.2. Phylogenetic relationships between SHBV, known hepadnaviruses and Carvalho Dominguez Souza et al., 2018). Importantly, a phylogeneti- their hosts cally distinct virus harboured by tent-making bats (TBHBV) has the ability to infect human hepatocytes (Drexler et al., 2013). Interestingly, Although these viruses were discovered in three species of shrews at those viruses harboured by rodents, woolly monkey, capuchin monkey two distant sample sites (~1200 km), they were relatively closely to and tent-making bat were all identified in New World species (Rasche each other, with 91.3–99.8% nucleotide sequence similarity at the et al., 2016). genome level, and 90.8–99.8%, 93.2–100%, 92.7–99.9% and Shrews are small, mouse/mole-like mammals that belong to the 92.4–99.8% sequence similarity in the polymerase, core, surface and X family Soricidae (Mammalia: Eulipotyphla) that have a worldwide dis- genes, respectively. In marked contrast, these shrew viruses exhibited tribution, and are also one of the largest and most abundant mamma- more than 50% genome divergence compared to all known hepadna- lian groups (Wilson and Reeder, 2005). While rodents and bats are viruses (Table 3). Together with the phylogenetic analyses (see below), recognised as important hosts of zoonotic pathogens, including lassa- these results showed that the shrew viruses discovered in this study virus (Smith and Wang, 2013), filoviruses (Smith and Wang, 2013), were distinct from the known orthhepadnaviruses, such that they re- hantaviruses (Guo et al., 2013) and coronaviruses (Wang et al., 2015; present a new member of the genus Orthohepadnavirus. Following the Lin et al., 2017; Woo et al., 2012), relatively little is known about the naming tradition of a new orthohepadnaviruses we named these as role played by shrews in shaping virus diversity, evolution and trans- representatives of shrew hepatitis B virus (SHBV) based on its host mission. Recently, several viruses - arenaviruses (Li et al., 2015), cor- association. onaviruses (Wang et al., 2017b), hantaviruses (Lin et al., 2014; Radosa To better understand the evolutionary relationship of SHBV with et al., 2013; Zhang, 2014) and rotaviruses (Li et al., 2016) - have been other orthohepadnaviruses, we estimated phylogenetic trees of full discovered in shrews. The shrew arenavirus is particularly important as length of genome, the polymerase, surface protein and core protein it is considered a zoonotic pathogen that could infect humans causing using a Maximum Likelihood (ML) method (Fig. 2 and Fig. 3) and fever and respiratory symptoms (Blasdell et al., 2016). Hence, shrews utilizing the hepadnavirus from bluegill (Dill et al., 2016) as an out- may be key hosts for a diversity of RNA viruses of which only a tiny group as it is the virus most closely related to the orthohepadnaviruses. proportion have been sampled to date (Wang et al., 2017b), but have In the full genome tree (Fig. 2), SHBVs and other orthohepadnaviruses been largely neglected as reservoirs for infectious
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