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Detection and Characterization of a Novel Norovirus in Bats, China

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Detection and Characterization of a Novel Norovirus in Bats, China Virologica Sinica (2018) 33:100–103 www.virosin.org https://doi.org/10.1007/s12250-018-0010-9 www.springer.com/12250 (0123456789().,-volV)(0123456789().,-volV) LETTER Detection and Characterization of a Novel Norovirus in Bats, China Ling’en Yang1,2 · Quanxi Wang1 · Lin Xu2 · Changchun Tu1,2,3 · Xiaohong Huang1 · Biao He2,3 Received: 7 November 2017 / Accepted: 21 December 2017 © Wuhan Institute of Virology, CAS and Springer Nature Singapore Pte Ltd. 2018. This article is an open access publication Dear Editor, found in GI, GII and GIV, while porcine NoVs group in distinct genotypes within GII, bovine and ovine viruses Noroviruses (NoVs) are second only to the rotaviruses as belong exclusively to GIII, murine NoVs are grouped in etiologic agents of acute fulminant gastroenteritis in infants GV, canine NoVs are in GIV and GVI, and lion viruses and young children worldwide, with an estimated 200,000 have been found only in GIV (Green 2013). deaths per year in children younger than 5 years of age in As one of the most widely distributed mammals, bats are developing countries (Patel et al. 2008). NoVs are classi- important natural reservoirs of viruses, of which more than fied within the genus Norovirus of the family Caliciviridae 137 have been discovered (Luis et al. 2013), including with Norwalk virus as its prototype member (ICTV 2017). many highly pathogenic agents such as Hendra and Nipah The virions are small (38–40 nm in diameter) nonen- viruses (Yob et al. 2001), SARS-related coronaviruses (Ge veloped, with an icosahedral capsidanda linear, positive- et al. 2013), and Marburg virus (Amman et al. 2012; sense, single-stranded, 7.7 kb RNA genome that is orga- Towner et al. 2009). Bats have also been found to harbor nized into 3 open-reading frames (ORF) (Green 2013). diverse caliciviruses, in countries including China, Hun- While only one species is currently recognized within the gary, and Cameroon, all showing close relationship with genus, molecular epidemiological studies have demon- members of the genus Sapovirus (Kemenesi et al. 2016; strated a marked genetic diversity among circulating NoVs, Tse et al. 2012), Nevertheless, only one sequence (acces- and genotyping has been proposed based on relatedness sion number: KJ790198) and several 660 nucleotides (nt) within the complete VP1 capsid protein (Green 2013). amplicons of bat-borne NoVs, from China, has been Such a system has divided members into 6 major phylo- reported (Hu et al. 2017). genetic clades or genogroups, designated GI through GVI In 2016, 178 adult bats were collected from Yanshi, Shawu and sharing 46.1%–58.8% nucleotide (nt) identities in their and Nanping in Fujian province, southeast China. The col- VP1 gene. Clades GI, II, and III are further subdivided into lection comprised 4 species: Rhinolophus sinicus (Yanshi, 9, 21, and 3 genotypes, respectively, indicating the need for n = 48; Nanping, n = 1), Hipposideros armiger (Nanping, further characterization of species criteria (Green 2013). n = 10), Rhinolophus affinis (Nanping, n = 62; Shawu, NoVs have been detected in a number of mammalian n = 21), and Myotis horsfieldii (Shawu, n = 36) (Fig. 1A). All species (De Graaf et al. 2017). Strains infecting humans are bats were live-captured with nets near or within human inhabited communities, and were apparently healthy at cap- Ling’en Yang and Quanxi Wang have contributed equally to this ture. Anal specimens were collected using sterile swabs, work. immediately transferred to viral transport medium, and stored & Xiaohong Huang in liquid nitrogen after sample collection, as described pre- [email protected] viously (He et al. 2017). As part of another investigation, all & Biao He were tested for group A rotaviral RNA and found negative. [email protected] Samples from each location were pooled and subjected to viral 1 metagenomic analysis as per our published method (He et al. College of Animal Science, Fujian A & F University, 2013).Ten contigs were annotated to NoVs, with an average Fuzhou 350002, China 2 length of 189 nt and showing 68%–79% nt sequence identity Key Laboratory of Jilin Province for Zoonosis Prevention and with other known NoVs, these were used to design PCR pri- Control, Military Veterinary Institute, Academy of Military Medical Sciences, Changchun 130122, China mers, targeting 239 nt of the polyprotein gene (forward primer 3 sequence: 5′-CAACTGTGACCGCATAGAG-3′;reverse Jiangsu Co-innovation Center for Prevention and Control of ′ ′ Important Animal Infectious Diseases and Zoonosis, primer sequence: 5 -TGAGGACGAGGTGGGAATG-3 ). Yangzhou 225009, China RNA of the samples was extracted using QIAamp RNA Mini 123 L. Yang et al.: Novel bat noroviruses, China 101 A 13 6: <6 NP B 97 EF439956 Hu/NoV/GI.4/Chiba 407/1987/JP C 83 AJ277614.1 HU/NLV/GI.5/Musgrove/1989/UK L07418.1 Hu/NoV/GI.2/Southampton/1991/UK 93 AF093797 Hu/NoV/GI.6/Hesse 3 (BS5)/1997/DE Genogroup 䊠 100 M87661.2 Hu/NoV/GI.1/Norwalk/1968/US U04469.1 Hu/NoV/GI.3/Desert Shield 395/1990/SA 99 99 AJ277609.1 HU/NoV/GI.7/Winchester/1994/UK AF538679.1 Hu/NoV/GI.8/Boxer/2001/US AJ011099.1 Bo/NoV/GIII.1/Jena/1980/DE 100 FJ946859.1 Bo/NoV/GIII/BV416/2008/BEL Genogroup 䊢 88 100 AF320625.1 Bo/NoV/GIII.2/CH126/1998/NL 100 AF195847.1 Hu/NoV/GIV.1/Alphatron/1998/NET Genogroup 䊣 75 JF781268 Cat/NoV/GIV.2/CU081210E/2010/USA Norovirus KT245136.1 Cat/NoV/GVI.2/TE/2013/ITA Genogroup 䊥 99 AF195848.1 Hu/NoV/GII.8/Amsterdam/1998/NL U02030.1 Hu/NoV/GII.3/Toronto 24/1991/CA 100 100 99 U07611.2 Hu/NoV/GII.1/Hawaii/1971/US Genogroup 䊡 HQ401025.1 Hu/NoV/GII.12/HS207/2010/USA 99 X81879.1 Hu/NoV/GII.2/Melksham/1994/UK AF427118.1 Hu/NoV/GII.10/Erfurt/546/2000/DE 100 MF373609 Bt/NoV/Fujian/2016/CHN Genogroup 䊦 KJ790198.1 Bt/NoV/YN/2010/CHN 99 JQ658375.1 Mu/NoV/GV/MNV3/2007/USA 100 NC008311 Mu/NoV/GV/MNV1/2003/USA Genogroup 䊤 AB601769.1 Mu/NoV/GV/MNV/2008/JP NC001543 Ra/RHDV/FRG/USA Lagovirus Lagovirus JX018212.1 Bo/NBV/M3641/2011/HUN Nebovirus Nebovirus 100 KX371573 Cat/VeV/WZ-1/CHN Vesivirus Vesivirus KX759620.1 Bt/SaV/Limbe65/2014/CAM 100 AT306742 Hu/SaV/GII.8/Peru-143/2009/PER 100 AY603425 Hu/SaV/Sakai/2001/JP 99 AJ950882 Mu/SaV2/Manhattan/2013/USA Spaovirus Spaovirus 100 AU712497 Bt/CalV/M63/2013/HUN 85 AJ641703 Bt/CalV/JX/2010/CHN 95 JN899072 Bt/SaV/TLC34/2012/HK 98 KJ641701 Bt/CalV/GX/2012/CHN 0.1 Fig. 1 A Sampling location of this study, filled circles: bats positive NPIH26 (filled red circle) and representatives of other caliciviruses for norovirus; open circles: negative. B Genomic structural schematic based on their complete VP1 amino acid sequences. Other bat-borne representation of NPIH26. Boxes represent the open reading frames caliciviruses are indicated by filled black triangles. Genogroups within encoding main proteins, nonstructural protein (39–4907 nt), VP1 the genus Norovirus are shown next to brackets, with the new (4891–6492 nt) and VP2 (6489–7268 nt). C Phylogenetic analysis of genotype proposed in this study in red. 123 102 Virologica Sinica Kit (Qiagen, Hilden, Germany), and subjected to RT-PCR MEGA6, and a phylogenetic tree was constructed by the screening, with 35 circles of 94 °C for 30 s, 58 °Cfor30sand maximum likelihood and general time reversible models 72 °C for 30 s. RT-PCR with double-distilled water replacing under evaluation of 1000 bootstraps. The viruses clustered the RNA was included as a negative control. Results showed within five groups corresponding to their genera within the that 2 of 62 (3.2%) R. affinis collected from Nanping were family Caliciviridae, with NPIH26 placed with other NoVs positive. Preliminary phylogenetic inspection of the ampli- but forming a phylogenetic group with BtRs-CalV/YN2010 cons showed that they shared 99.8% nt identity, and the separate from the six currently known genogroups. viruses from which they originated were named NPIH26 and Accordingly, these bat-borne NoVs can be considered as NPIH29. The genomic sequence of NPIH26 was then deter- comprising a new genogroup, GVII (Fig. 1C). ORF1 and mined using a long-range PCR system (TaKaRa, Dalian, VP2 were also used for phylogenetic analyses and showed China) and Rapid Amplification of cDNA Ends (RACE, similar topology with that of VP1 (data not shown). TaKaRa). Results showed that the complete genome (Gen- Kunming mice (3 day-old) were inoculated intraorally Bank accession number: MF373609) was 7368 nt in length with positive sample NPIH26 for virus isolation with daily with 58.05% CG content and possessed genomic organization inspection for any visible pathology. At 7 days, without typical of noroviruses, containing three ORFs encoding the showing any signs of morbidity or weight loss, all mice multifunctional nonstructural protein, VP1 and VP2, as well were euthanized and their organs (intestines with contents, as 5′ leader and 3′ trailer sequences (38 and 33 nt respectively) lungs, livers, kidneys and spleens) were removed and (Fig. 1B). The conserved motifs DYXX(TR)WDST, GLPSG subjected to specific RT-PCR detection. All organs tested and YGDD were observed and the genome contained the same negative for this virus. structures in the RNA-dependent RNA polymerase region as Of all the noroviruses, only murine strains have been other NoVs (Kemenesi et al. 2016;Smileyetal.2002;Wolf propagated in cell culture. Consequently, the inability to et al. 2011). cultivate human NoVs in vitro has been a major obstacle to Genomic comparison with representatives of the six the development of antivirals and vaccines to cure or pre- NoV genogroups and other caliciviruses showed that vent human noroviral diseases (Green 2013).
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