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Isolation and genetic characterization of a mammalian orthoreovirus from Vespertilio sinensis in Japan

Isolation and genetic characterization of a mammalian orthoreovirus from Vespertilio sinensis in... Throughout East Asia, Europe, and North America, mammalian orthoreovirus (MRV), for which bats have been proposed to be natural reservoirs, has been detected in a variety of domestic and wild mammals, as well as in humans. Here, we isolated a novel MRV strain (designated as Kj22-33) from a fecal sample from Vespertilio sinensis bats in Japan. Strain Kj22-33 has a 10-segmented genome with a total length of 23,580 base pairs. Phylogenetic analysis indicated that Kj22-33 is a serotype 2 strain, the segmented genome of which has undergone reassortment with that of other MRV strains. Reoviruses, members of the order Reovirales, are classified capsid protein σ1 plays a role in cell attachment and is the into two families, namely, Sedoreoviridae and Spinareoviri- only determinant distinguishing the serotypes. dae, each of which comprises several genera. Organisms Since its initial isolation from the stools of children in within a diverse spectrum of taxonomic groups, including 1954 [1], MRV has been reported in children with gastroen- protists, plants, fish, amphibians, birds, and mammals, serve teritis [3–5]. In addition, strains of MRV have been detected as hosts for viruses from both of these families. Mammalian continually in a wide range of mammals, including pigs [6], orthoreovirus is one of the 10 species comprising the genus wild boars [7], cats [8], dogs [9], bats [10–17], and deer Orthoreovirus within the family Spinareoviridae, and it [18], and have also been found in wastewater [19], indicat- can be further divided into four major serotypes (MRV1–4) ing the broad host range of this virus. Bats are particularly based on antigenicity in neutralization and hemagglutination noteworthy in this regard, in that they are considered to be inhibition tests [1, 2]. natural reservoirs of MRV, and a genetically diverse range Mammalian orthoreovirus (MRV) is a non-enveloped of strains have been detected in different bat species [10]. virus with a 10-segmented double-stranded RNA genome However, although bat MRVs have been reported in mul- consisting of three large (L1–L3), three medium (M1–M3), tiple regions, including Europe [9, 11], the United States and four small (S1–S4) segments. The L1, L2, L3, M1, M2, [13], China [10, 14–16], and Korea [17], to date, none of S1, S2, and S4 segments encode eight structural proteins these viruses have been detected in Japanese bats, despite (λ1, λ2, λ3, µ1, µ2, σ1, σ2, and σ3, respectively), whereas the presence of MRV in several mammals in Japan [6–9]. the M3 segment encodes two non-structural proteins (µNS In this study, we detected and isolated a novel MRV strain and µNSC), and the S1 and S3 segments each encode a non- from bats in Japan. structural protein (σ1s and σNS, respectively). The external To determine whether bat MRVs are present in Japan, in July 2022, we collected fecal samples from Asian par- ticolored bats (Vespertilio sinensis) in Saitama Prefecture, Handling Editor: Zhenhai Chen. Japan. Suspensions of the collected feces were subsequently used to inoculate Vero cells expressing transmembrane ser- * Shin Murakami ine protease 2 (Vero/TMPRSS2), which may support the shin-murakami@g.ecc.u-tokyo.ac.jp replication of unknown viruses, including MRVs [20]. Sekine Wataru The inoculated cells were incubated at 37℃ in a 5% C O w-sekine@g.ecc.u-tokyo.ac.jp atmosphere, and at 3 days post-inoculation, we observed Laboratory of Veterinary Microbiology, Graduate School a clear cytopathic effect (CPE). The cell supernatant was of Agricultural and Life Sciences, The University of Tokyo, passed through a 0.22-µm-pore-size filter, and the filtrate 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan Vol.:(0123456789) 1 3 165 Page 2 of 5 A. Ichikawa et al. Table 1 Mammalian Segment % Identity Serotype Strain Host Country Year Accession no. orthoreovirus strains with the highest sequence similarity to L1 98.3 T2 17-EF40 Bat USA 2017 MW718862 each genome segment of Kj22- L2 98.5 T2 WIV4 Bat China 2011 KT444533 33 by NCBI BLAST search L3 98.9 T2 OV204 Deer USA 2016 MK092966 M1 98.0 T1 B19-02 Bat South Korea 2019 MW582625 M2 99.2 T1 B19-02 Bat South Korea 2019 MW582626 M3 99.0 T2 WIV3 Bat China 2011 KT444577 S1 96.2 T2 RpMRV-YN2012 Bat China 2012 KM087111 S2 98.5 T2 OV204 Deer USA 2016 MK092971 S3 99.1 T3 SD-14 Mink China 2014 KT224512 S4 99.5 T2 WIV5 Bat China 2011 KT444551 was used inoculate fresh Vero/TMPRSS2 cells. Consistently, of Kj22-33 appears to be closely related to that of the we observed a CPE, thereby confirming the isolation of a strain MRV2/RpMRV-YN2012/bat/2012/China (YN2012), virus (hereafter referred to as Kj22-33). To identify the viral the other segments of Kj22-33 were observed to cluster genome type, we used two antiviral drugs – ribavirin and in clades distant from that containing YN2012. MRV2/ 5-iodo-2ʹ-deoxyuridine (IUDR) – which inhibit the growth OV204/deer/2016/USA showed the highest nucleotide of RNA and DNA viruses, respectively. Viral growth was sequence similarity in the L3 and S2 genomic segments, found to be inhibited only in the presence of ribavirin, indi- but it also exhibited phylogenetic relatedness in the S2, cating that Kj22-33 has an RNA genome. S3, M3, L1, and L3 segments, suggesting an evolutionary We purified the Kj22-33 isolate from the infected cell association among these genomic segments. These find- supernatant by ultracentrifugation with a 20% sucrose ings suggest that Kj22-33 may have arisen as a conse- cushion and extracted the RNA using ISOGEN-LS (Nip- quence of genomic reassortment with the closely related pon Gene, Toyama, Japan). An MGIEasy RNA Directional YN2012 and OV204 strains, as well as others. Library Prep Set (MGI, Shenzhen, China) was used to pre- In general, viruses exhibit a high degree of host speci- pare a library for genome sequencing using a DNBSEQ ficity and are able to infect only a narrow range of hosts. G400RS high-throughput sequencer (MGI, Shenzhen, In contrast, MRV has been established to have low host China). The dataset thus obtained was assembled de novo specificity and is accordingly characterized by a broad using CLC Genomics Workbench software (ver. 8; CLCbio, host range. In this study, we conducted a comprehensive Aarhus, Denmark), and accordingly, we obtained sequences phylogenetic analysis of all genomic segments and found for 10 segments. The 5ʹ and 3ʹ regions of each segment were that although segment S1 of the Kj22-33 isolate is closely subsequently determined by RACE (rapid amplification of related to the corresponding segment of the YN2012 strain cDNA ends) using a SMARTer RACE 5'/3' Kit (Takara obtained from Chinese bats, five out of the ten segments Bio, Shiga, Japan), on the basis of which we determined the of Kj22-33 were most closely related to those of MRV full viral genome sequence (GenBank accession numbers identified in white-tailed deer in the USA, despite the large LC752173–LC752182). NCBI BLAST searches revealed geographical distance. Given that the host of Kj22-33, that all 10 segments showed high similarity (96.2% to 99.5% the bat Vespertilio sinensis, is a common species in East identity) to the genomic sequences of MRV strains isolated Asia, and that it inhabits an environment quite distinct from different animal species (Table  1). from that of the white-tailed deer, the reason for the appar- Phylogenetic analysis was performed based on ently close relationship between these two geographically sequences of each Kj22-33 genome segment (Fig. 1). Trees distant viruses remains unclear. Moreover, given its low were constructed using the maximum-likelihood method host specificity, the global distribution and epidemiology based on the Tamura-Nei model in MEGA X [21]. The S1 of MRV remains largely undetermined, and further studies sequence of Kj22-33 was found to group in the same clade are therefore required to clarify its mode of spread. as serotype 2 strains. However, although the S1 segment 1 3 A mammalian orthoreovirus from Vespertilio sinensis in Japan Page 3 of 5 165 S2 segment S1 segment Fig. 1 Phylogenetic analysis Kj22-33/bat/2022/Japan 83 96 MRV2/WIV3/bat/2011/China_KT444579 MRV2/RpMRV-YN2012/bat/2012/China_ KM087111 100 MRV1/HLJYC2017/swine/2017/China_MN788301 MRV2/OV204/deer/2016/USA_MK092970 of the 10 genome segments of MRV1/WIV2/2007/China_KT444529 94 MRV2/sR1521/pig/2015/Taiwan_LC482234 MRV1/THK0617/wastewater/2020/Japan_LC613228 MRV2/WIV3/bat/2011/China_KT444578 99 MRV2/Osaka2005/human/2005/Japan_LC476912 strain Kj22-33. Phylogenetic 100 MRV2/WIV4/bat/2011/China_KT444538 MRV2/115/bat/2017/USA_OP019320 MRV2/THK0325/wastewater/2020/Japan_LC613218 MRV2/SI-MRV05/bat/2008/Slovenia_MG457114 MRV2/WIV4/bat/2011/China_KT444539 trees were constructed by the MRV2/WIV5/bat/2011/China_KT444548 98 MRV3/SD-14/mink/2014/China_KT224511 MRV2/THK0325/wastewater/2020/Japan_LC613215 98 MRV2 Kj22-33/bat/2022/Japan MRV2/Osaka2005/human/2005/Japan_LC476911 MRV2/OV204/deer/2016/USA_MK092971 maximum-likelihood method MRV2/Osaka2014/human/2014/Japan_LC476921 99 84 MRV1/40/bat/2018/USA_OP057401 MRV2/Osaka1994/human/1994/Japan_LC476901 MRV2/17-EF40/bat/2017/USA_MW718868 MRV1/B19-02/bat/2019/South Korea_MW582629 with 1,000 bootstrap replicates 100 MRV2/18RS290002/bat/2018/Italy_MW199193 96 MRV2/17-EF40/bat/2017/USA_MW718869 37 MRV2/809/bat/2017/USA_ OP057390 MRV4/Ndelle/mouse/1974/Cameroon_AF368036 51 MRV2/19/242/mouse/2019/Germany_MN639761 MRV1/466/bat/2017/USA_OP057379 using MEGA X software. 92 86 MRV2/5515-3/bat/2011/Italy_KU194672 100 MRV2/115/bat/2017/USA_OP037826 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900701 MRV3/SI-MRV01/human/2013/Slovenia_KF154731 100 MRV1/HB-A/mink/2013/China_KC462155 The numbers at nodes denote MRV1/WIV8/bat/2011/China_KT444568 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900702 99 100 99 70 MRV1/THK0617/wastewater/2020/Japan_LC613225 MRV2/RpMRV-YN2012/bat/2012/China_ KM087112 99 MRV1/WIV2/bat/2007/China_KT444528 MRV1 MRV3/342/bat/2008/Germany_ JQ412762 bootstrap values based on 1000 100 MRV1/B19-02/bat/2019/South Korea_MW582628 MRV2/809/bat/2017/USA_ OP057391 96 MRV1/HLJYC2017/swine/2017/China_MN788300 86 MRV2/Osaka1994/human/1994/Japan LC476902 MRV1/40/bat/2018/USA_ OP057400 replicates. The scale bar shows 100 MRV2/Osaka2014/human/2014/Japan_ LC476922 MRV1/466/bat/2017/USA_ OP057378 MRV4/Ndelle/mouse/1974/Cameroon_ AF368035 Avian orthoreovirus_HM222973 MRV4 MRV3/SD-14/mink/2014/China_KT224510 NelsonBay_AF059722 the evolutionary distance in 100 99 MRV3/WIV7/bat/2011/China_KT444558 MRV3/T3D/human/2002/USA_HM159619 0.50 96 MRV3/T3/206645-31/2011/Italy_JQ979275 terms of nucleotide substitu- MRV3 MRV3/342/bat/2008/Germany_JQ412761 MRV3/SI-MRV01/human/2013/Slovenia_KF154730 MRV3/Sl-MRV02/bat/2010/Slovenia_MG457084 tions per site. The virus strain NelsonBay_AF218360 Avian orthoreovirus_HM222974 Kj22-33 is shown in bold red. 0.50 Virus strains are labeled as S3 segment S4 segment MRV2/17-EF40/bat/2017/USA_MW718870 89 Kj22-33/bat/2022/Japan follows: MRV serotype/strain MRV2/809/bat/2017/USA_OP057392 MRV2/THK0325/wastewater/2020/Japan_LC613216 91 MRV3/SD-14/mink/2014/China_KT224512 MRV2/WIV3/bat/2011/China_ KT444581 MRV2/THK0325/wastewater/2020/Japan_LC613217 name/detection host or material/ MRV1/HLJYC2017/swine/2017/China_MN788303 MRV2/OV204/deer/2016/USA_MK092972 90 MRV1/B19-02/bat/2019/South Korea_MW582631 Kj22-33/bat/2022/Japan MRV1/THK0617/wastewater/2020/Japan_LC613226 detection year/country/GenBank MRV2/Osaka2014/human/2014/Japan_LC476923 81 MRV1/WIV2/bat/2007/China_KT444531 MRV2/Osaka1994/human/1994/Japan_LC476903 99 MRV2/WIV4/bat/2011/China_KT444541 MRV2/WIV4/bat/2011/China_KT444540 MRV2/Osaka2005/human/2005/Japan_LC476914 accession number. The four MRV2/Osaka2005/human/2005/Japan_LC476913 MRV2/OV204/deer/2016/USA_MK092973 MRV1/WIV2/bat/2007/China_KT444530 97 100 MRV3/SD-14/mink/2014/China_KT224513 99 MRV2/WIV3/bat/2011/China_KT444580 serotype groups are indicated MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900704 MRV1/HLJYC2017/swine/2017/China_MN788302 MRV2/809/bat/2017/USA_OP057393 78 MRV1/B19-02/bat/2019/South Korea_MW582630 98 MRV2/Osaka1994/human/1994/Japan_LC476904 MRV1/40/bat/2018/USA_OP057402 88 on the right-hand side of the S1 48 37 100 MRV1/466/bat/2017/USA_OP057380 99 MRV2/Osaka2014/human/2014/Japan_LC476924 MRV2/115/bat/2017/USA_OP037827 23 MRV2/17-EF40/bat/2017/USA_MW718871 MRV1/THK0617/wastewater/2020/Japan_LC613227 segment tree. 43 MRV1/40/bat/2018/USA_OP057403 MRV2/RpMRV-YN2012/bat/2012/China_KM087113 MRV4/Ndelle/mouse/1974/Cameroon_AF368037 MRV3/342/bat/2008/Germany_JQ412763 MRV2/RpMRV-YN2012/bat/2012/China_KM087114 MRV3/SI-MRV01/human/2013/Slovenia_KF154732 100 MRV3/342/bat/2008/Germany_JQ412764 NelsonBay_AF059726 99 MRV3/SI-MRV01/human/2013/Slovenia_KF154733 Avian orthoreovirus_HM222972 MRV1/466/bat/2017/USA_OP057381 100MRV2/115/bat/2017/USA_OP037828 0.50 NelsonBay_NC038658 Avian orthoreovirus_HM222971 0.50 M1 segment M2 segment 100 MRV2/17-EF40/bat/2017/USA_MW718868 88 MRV1/HLJYC2017/swine/2017/China_MN788298 MRV2/809/bat/2017/USA_ OP057394 MRV2/THK0325/wastewater/2020/Japan_LC613213 99 100 MRV2/809/bat/2017/USA_ OP057395 MRV3/SD-14/mink/2014/China_KT224507 54 MRV2/OV204/deer/2016/USA_MK092968 MRV2/Osaka2005/human/2005/Japan_LC476908 81 85 MRV3/SD-14/mink/2014/China_KT224508 MRV2/Osaka1994/human/1994/Japan_LC476898 MRV2/WIV4/bat/2011/China_ KT444536 98 MRV2/WIV4/bat/2011/China_ KT444535 MRV2/Osaka2014/human/2014/Japan_ LC476919 MRV2/Osaka2014/human/2014/Japan_ LC476918 86 81 MRV2/Osaka1994/human/1994/Japan_ LC476899 MRV2/THK0325/wastewater/2020/Japan_LC613212 79 MRV2/Osaka2005/human/2005/Japan_ LC476909 MRV1/THK0617/wastewater/2020/Japan_LC613222 93 77 MRV2/RpMRV-YN2012/bat/2012/China_ KM087109 MRV2/RpMRV-YN2012/bat/2012/China_KM087108 MRV3/342/bat/2008/Germany_ JQ412757 MRV1/WIV2/bat/2007/China_KT444525 85 MRV3/SI-MRV01/human/2013/Slovenia_KF154728 MRV2/WIV3/bat/2011/China_ KT444575 60 MRV1/40/bat/2018/USA_ OP057405 94 MRV1/WIV2/bat/2007/China_ KT444526 99 MRV1/HLJYC2017/swine/2017/China_MN788297 MRV2/WIV3/bat/2011/China_ KT444576 64 MRV1/466/bat/2017/USA_OP057382 MRV1/BatMRV1-IT2011/bat/2011/Italy_ KT900699 100 MRV2/115/bat/2017/USA_OP037829 75 MRV4/Ndelle/mouse/1974/Cameroon_ AF368034 MRV1/40/bat/2018/USA_ OP057404 100 MRV2/17-EF40/bat/2017/USA_MW718866 100 56 Kj22-33/bat/2022/Japan MRV1/THK0617/wastewater/2020/Japan_LC613223 98 MRV1/B19-02/bat/2019/South Korea_ MW582625 Kj22-33/bat/2022/Japan MRV2/OV204/deer/2016/USA_MK092967 99 MRV1/B19-02/bat/2019/South Korea_ MW582626 MRV1/BatMRV1-IT2011/bat/2011/Italy_ KT900698 MRV2/115/bat/2017/USA_OP037830 MRV3/342/bat/2008/Germany_ JQ412758 100 MRV1/466/bat/2017/USA_ OP057383 95 MRV3/SI-MRV01/human/2013/Slovenia_KF154727 NelsonBay_LC619333 Avian orthoreovirus_HM222976 Avian orthoreovirus_HM222977 NelsonBay_LC619332 0.10 0.20 M3 segment L1 segment MRV2/WIV3/bat/2011/China_ KT444577 MRV2/17-EF40/bat/2017/USA_MW718862 MRV2/809/bat/2017/USA_OP57397 86 MRV2/OV204/deer/2016/USA_MK092969 MRV2/THK0325/wastewater/2020/Japan_LC613209 Kj22-33/bat/2022/Japan 89 Kj22-33/bat/2022/Japan MRV1/HLJYC2017/swine/2017/China_MN788299 99 MRV2/OV204/deer/2016/USA_MK092964 MRV3/SD-14/mink/2014/China_KT224509 MRV3/SD-14/mink/2014/China_KT224504 MRV2/17-EF40/bat/2017/USA_ MW718867 MRV2/WIV4/bat/2011/China_KT444532 MRV2/THK0325/wastewater/2020/Japan_LC613214 MRV1/THK0617/wastewater/2020/Japan_LC613219 MRV2/WIV4/bat/2011/China_ KT444537 MRV2/Osaka2005/human/2005/Japan_LC476905 MRV2/809/bat/2017/USA_ OP057396 97 MRV2/Osaka1994/human/1994/Japan_LC476895 MRV2/Osaka2005/human/2005/Japan_ LC476910 95 99 MRV2/Osaka2014/human/2014/Japan_LC476915 97 MRV1/WIV2/bat/2007/China_KT444537 MRV1/B19-02/bat/2019/South Korea_MW58262 MRV1/THK0617/wastewater/2020/Japan MRV1/466/bat/2017/USA_OP057385 96 MRV1/B19-02/bat/2019/South Korea_ MW582627 MRV2/115/bat/2017/USA_OP037832 MRV1/40/bat/2018/USA_ OP057406 MRV2/RpMRV-YN2012/bat/2012/China_KM087105 MRV1/BatMRV1-IT2011/bat/2011/Italy_ KT900700 MRV4/Ndelle/mouse/1974/Cameroon_AF368033 1 MRV2/RpMRV-YN2012/bat/2012/China_ KM087110 MRV1/40/bat/2018/USA_OP057407 99 MRV3/342/bat/2008/Germany_ JQ412760 38 100 MRV3/342/bat/2008/Germany_ JQ412755 MRV3/SI-MRV01/human/2013/Slovenia_ KF154729 MRV3/SI-MRV01/human/2013/Slovenia_KF154724 54 MRV1/466/bat/2017/USA_OP057384 100 100 MRV1/WIV2/bat/2007/China_KT444522 MRV2/115/bat/2017/USA_ OP037831 MRV2/WIV3/bat/2011/China_KT444572 MRV2/Osaka2014/human/2014/Japan_ LC476920 MRV1/HLJYC2017/swine/2017/China_MN788294 MRV2/Osaka1994/human/1994/Japan_ LC476900 NelsonBay_LC619329 NelsonBay_LC619334 Avian orthoreovirus_HM22978 Avian orthoreovirus_HM222975 0.20 0.20 L2 segment L3 segment 99 Kj22-33/bat/2022/Japan Kj22-33/bat/2022/Japan 99 MRV2/WIV4/bat/2011/China_KT444533 MRV2/OV204/deer/2016/USA_MK092966 MRV2/Osaka2005/human/2005/Japan_LC476906 MRV2/17-EF40/bat/2017/USA_MW718864 100 97 MRV1/HB-A/mink/2013/China_KC462150 MRV2/809/bat/2017/USA_OP057399 MRV2/Osaka1994/human/1994/Japan_LC47896 MRV1/HLJYC2017/swine/2017/China_MN788296 MRV2/Osaka2014/human/2014/Japan_LC476916 99 MRV2/Osaka2005/human/2005/JapanLC476907 98 MRV2/WIV3/bat/2011/China_KT444573 MRV1/WIV2/bat/2007/China_KT444524 MRV1/HLJYC2017/swine/2017/China_MN788295 MRV3/SD-14/mink/2014/China_KT224506 MRV1/WIV2/bat/2007/China_KT444523 MRV2/Osaka2014/human/2014/Japan_LC476917 MRV1/THK0617/wastewater/2020/Japan_LC613220 81 MRV1/HB-A/mink/2013/China_KC462151 99 MRV2/17-EF40/bat/2017/USA_MW718863 97 MRV2/WIV3/bat/2011/China_KT444574 87 MRV2/bat/2017/USA_OP057398 MRV2/THK0325/wastewater/2020/Japan_LC613211 MRV2/19/242/mouse/2019/Germany_MN639756 100 98 MRV2/WIV4/bat/2011/China_KT444534 MRV2/THK0325/wastewater/2020/Japan_LC613210 100 98 MRV2/Osaka1994/human/1994/Japan_ LC476897 MRV2/OV204/deer/2016/USA_MK092965 67 99 MRV1/THK0617/wastewater/2020/Japan_LC613221 100 MRV3/SD-14/mink/2014/China_KT224505 MRV1/40/bat/2018/USA_OP057409 MRV2/115/bat/2017/USA_OP037833 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900697 100 MRV1/40/bat/2018/USA_OP057408 100 MRV1/466/bat/2017/USA_OP057387 MRV1/466/bat/2017/USA_OP057386 95 MRV2/115/bat/2017/USA_OP037834 MRV2/RpMRV-YN2012/bat/2012/China_KM087106 MRV1/B19-02/bat/2019/South Korea_MW582624 80 MRV1/B19-02/bat/2019/South Korea_MW582623 MRV2/RpMRV-YN2012/bat/2012/China_KM087107 97 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900696 MRV3/342/bat/2008/Germany_JQ412755 99 100 MRV3/342/bat/2008/Germany_JQ412756 MRV3/SI-MRV01/human/2013/Slovenia_KF154726 MRV3/SI-MRV01/human/2013/Slovenia_KF154725 NelsonBay_LC619331 NelsonBay_LC619330 Avian orthoreovirus_HM222979 Avian orthoreovirus_HM222980 0.20 0.20 1 3 165 Page 4 of 5 A. 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Arch Virol Open Access This article is licensed under a Creative Commons Attri- 165:1541–1550. https:// doi. org/ 10. 1007/ s00705- 020- 04635-1 bution 4.0 International License, which permits use, sharing, adapta- 11. Lelli D, Moreno A, Lavazza A, Bresaola M, Canelli E, Boniotti tion, distribution and reproduction in any medium or format, as long MB, Cordioli P (2013) Identification of mammalian orthoreovirus as you give appropriate credit to the original author(s) and the source, type 3 in Italian bats. Zoonoses Public Health 60:84–92. https:// provide a link to the Creative Commons licence, and indicate if changes doi. org/ 10. 1111/ zph. 12001 were made. The images or other third party material in this article are 12. Naglič T, Rihtarič D, Hostnik P, Toplak N, Koren S, Kuhar U, included in the article's Creative Commons licence, unless indicated Jamnikar-Ciglenečki U, Kutnjak D, Steyer A (2018) Identifica - otherwise in a credit line to the material. 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Isolation and genetic characterization of a mammalian orthoreovirus from Vespertilio sinensis in Japan

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Springer Journals
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Copyright © The Author(s) 2023
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0304-8608
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1432-8798
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10.1007/s00705-023-05782-x
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Abstract

Throughout East Asia, Europe, and North America, mammalian orthoreovirus (MRV), for which bats have been proposed to be natural reservoirs, has been detected in a variety of domestic and wild mammals, as well as in humans. Here, we isolated a novel MRV strain (designated as Kj22-33) from a fecal sample from Vespertilio sinensis bats in Japan. Strain Kj22-33 has a 10-segmented genome with a total length of 23,580 base pairs. Phylogenetic analysis indicated that Kj22-33 is a serotype 2 strain, the segmented genome of which has undergone reassortment with that of other MRV strains. Reoviruses, members of the order Reovirales, are classified capsid protein σ1 plays a role in cell attachment and is the into two families, namely, Sedoreoviridae and Spinareoviri- only determinant distinguishing the serotypes. dae, each of which comprises several genera. Organisms Since its initial isolation from the stools of children in within a diverse spectrum of taxonomic groups, including 1954 [1], MRV has been reported in children with gastroen- protists, plants, fish, amphibians, birds, and mammals, serve teritis [3–5]. In addition, strains of MRV have been detected as hosts for viruses from both of these families. Mammalian continually in a wide range of mammals, including pigs [6], orthoreovirus is one of the 10 species comprising the genus wild boars [7], cats [8], dogs [9], bats [10–17], and deer Orthoreovirus within the family Spinareoviridae, and it [18], and have also been found in wastewater [19], indicat- can be further divided into four major serotypes (MRV1–4) ing the broad host range of this virus. Bats are particularly based on antigenicity in neutralization and hemagglutination noteworthy in this regard, in that they are considered to be inhibition tests [1, 2]. natural reservoirs of MRV, and a genetically diverse range Mammalian orthoreovirus (MRV) is a non-enveloped of strains have been detected in different bat species [10]. virus with a 10-segmented double-stranded RNA genome However, although bat MRVs have been reported in mul- consisting of three large (L1–L3), three medium (M1–M3), tiple regions, including Europe [9, 11], the United States and four small (S1–S4) segments. The L1, L2, L3, M1, M2, [13], China [10, 14–16], and Korea [17], to date, none of S1, S2, and S4 segments encode eight structural proteins these viruses have been detected in Japanese bats, despite (λ1, λ2, λ3, µ1, µ2, σ1, σ2, and σ3, respectively), whereas the presence of MRV in several mammals in Japan [6–9]. the M3 segment encodes two non-structural proteins (µNS In this study, we detected and isolated a novel MRV strain and µNSC), and the S1 and S3 segments each encode a non- from bats in Japan. structural protein (σ1s and σNS, respectively). The external To determine whether bat MRVs are present in Japan, in July 2022, we collected fecal samples from Asian par- ticolored bats (Vespertilio sinensis) in Saitama Prefecture, Handling Editor: Zhenhai Chen. Japan. Suspensions of the collected feces were subsequently used to inoculate Vero cells expressing transmembrane ser- * Shin Murakami ine protease 2 (Vero/TMPRSS2), which may support the shin-murakami@g.ecc.u-tokyo.ac.jp replication of unknown viruses, including MRVs [20]. Sekine Wataru The inoculated cells were incubated at 37℃ in a 5% C O w-sekine@g.ecc.u-tokyo.ac.jp atmosphere, and at 3 days post-inoculation, we observed Laboratory of Veterinary Microbiology, Graduate School a clear cytopathic effect (CPE). The cell supernatant was of Agricultural and Life Sciences, The University of Tokyo, passed through a 0.22-µm-pore-size filter, and the filtrate 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan Vol.:(0123456789) 1 3 165 Page 2 of 5 A. Ichikawa et al. Table 1 Mammalian Segment % Identity Serotype Strain Host Country Year Accession no. orthoreovirus strains with the highest sequence similarity to L1 98.3 T2 17-EF40 Bat USA 2017 MW718862 each genome segment of Kj22- L2 98.5 T2 WIV4 Bat China 2011 KT444533 33 by NCBI BLAST search L3 98.9 T2 OV204 Deer USA 2016 MK092966 M1 98.0 T1 B19-02 Bat South Korea 2019 MW582625 M2 99.2 T1 B19-02 Bat South Korea 2019 MW582626 M3 99.0 T2 WIV3 Bat China 2011 KT444577 S1 96.2 T2 RpMRV-YN2012 Bat China 2012 KM087111 S2 98.5 T2 OV204 Deer USA 2016 MK092971 S3 99.1 T3 SD-14 Mink China 2014 KT224512 S4 99.5 T2 WIV5 Bat China 2011 KT444551 was used inoculate fresh Vero/TMPRSS2 cells. Consistently, of Kj22-33 appears to be closely related to that of the we observed a CPE, thereby confirming the isolation of a strain MRV2/RpMRV-YN2012/bat/2012/China (YN2012), virus (hereafter referred to as Kj22-33). To identify the viral the other segments of Kj22-33 were observed to cluster genome type, we used two antiviral drugs – ribavirin and in clades distant from that containing YN2012. MRV2/ 5-iodo-2ʹ-deoxyuridine (IUDR) – which inhibit the growth OV204/deer/2016/USA showed the highest nucleotide of RNA and DNA viruses, respectively. Viral growth was sequence similarity in the L3 and S2 genomic segments, found to be inhibited only in the presence of ribavirin, indi- but it also exhibited phylogenetic relatedness in the S2, cating that Kj22-33 has an RNA genome. S3, M3, L1, and L3 segments, suggesting an evolutionary We purified the Kj22-33 isolate from the infected cell association among these genomic segments. These find- supernatant by ultracentrifugation with a 20% sucrose ings suggest that Kj22-33 may have arisen as a conse- cushion and extracted the RNA using ISOGEN-LS (Nip- quence of genomic reassortment with the closely related pon Gene, Toyama, Japan). An MGIEasy RNA Directional YN2012 and OV204 strains, as well as others. Library Prep Set (MGI, Shenzhen, China) was used to pre- In general, viruses exhibit a high degree of host speci- pare a library for genome sequencing using a DNBSEQ ficity and are able to infect only a narrow range of hosts. G400RS high-throughput sequencer (MGI, Shenzhen, In contrast, MRV has been established to have low host China). The dataset thus obtained was assembled de novo specificity and is accordingly characterized by a broad using CLC Genomics Workbench software (ver. 8; CLCbio, host range. In this study, we conducted a comprehensive Aarhus, Denmark), and accordingly, we obtained sequences phylogenetic analysis of all genomic segments and found for 10 segments. The 5ʹ and 3ʹ regions of each segment were that although segment S1 of the Kj22-33 isolate is closely subsequently determined by RACE (rapid amplification of related to the corresponding segment of the YN2012 strain cDNA ends) using a SMARTer RACE 5'/3' Kit (Takara obtained from Chinese bats, five out of the ten segments Bio, Shiga, Japan), on the basis of which we determined the of Kj22-33 were most closely related to those of MRV full viral genome sequence (GenBank accession numbers identified in white-tailed deer in the USA, despite the large LC752173–LC752182). NCBI BLAST searches revealed geographical distance. Given that the host of Kj22-33, that all 10 segments showed high similarity (96.2% to 99.5% the bat Vespertilio sinensis, is a common species in East identity) to the genomic sequences of MRV strains isolated Asia, and that it inhabits an environment quite distinct from different animal species (Table  1). from that of the white-tailed deer, the reason for the appar- Phylogenetic analysis was performed based on ently close relationship between these two geographically sequences of each Kj22-33 genome segment (Fig. 1). Trees distant viruses remains unclear. Moreover, given its low were constructed using the maximum-likelihood method host specificity, the global distribution and epidemiology based on the Tamura-Nei model in MEGA X [21]. The S1 of MRV remains largely undetermined, and further studies sequence of Kj22-33 was found to group in the same clade are therefore required to clarify its mode of spread. as serotype 2 strains. However, although the S1 segment 1 3 A mammalian orthoreovirus from Vespertilio sinensis in Japan Page 3 of 5 165 S2 segment S1 segment Fig. 1 Phylogenetic analysis Kj22-33/bat/2022/Japan 83 96 MRV2/WIV3/bat/2011/China_KT444579 MRV2/RpMRV-YN2012/bat/2012/China_ KM087111 100 MRV1/HLJYC2017/swine/2017/China_MN788301 MRV2/OV204/deer/2016/USA_MK092970 of the 10 genome segments of MRV1/WIV2/2007/China_KT444529 94 MRV2/sR1521/pig/2015/Taiwan_LC482234 MRV1/THK0617/wastewater/2020/Japan_LC613228 MRV2/WIV3/bat/2011/China_KT444578 99 MRV2/Osaka2005/human/2005/Japan_LC476912 strain Kj22-33. Phylogenetic 100 MRV2/WIV4/bat/2011/China_KT444538 MRV2/115/bat/2017/USA_OP019320 MRV2/THK0325/wastewater/2020/Japan_LC613218 MRV2/SI-MRV05/bat/2008/Slovenia_MG457114 MRV2/WIV4/bat/2011/China_KT444539 trees were constructed by the MRV2/WIV5/bat/2011/China_KT444548 98 MRV3/SD-14/mink/2014/China_KT224511 MRV2/THK0325/wastewater/2020/Japan_LC613215 98 MRV2 Kj22-33/bat/2022/Japan MRV2/Osaka2005/human/2005/Japan_LC476911 MRV2/OV204/deer/2016/USA_MK092971 maximum-likelihood method MRV2/Osaka2014/human/2014/Japan_LC476921 99 84 MRV1/40/bat/2018/USA_OP057401 MRV2/Osaka1994/human/1994/Japan_LC476901 MRV2/17-EF40/bat/2017/USA_MW718868 MRV1/B19-02/bat/2019/South Korea_MW582629 with 1,000 bootstrap replicates 100 MRV2/18RS290002/bat/2018/Italy_MW199193 96 MRV2/17-EF40/bat/2017/USA_MW718869 37 MRV2/809/bat/2017/USA_ OP057390 MRV4/Ndelle/mouse/1974/Cameroon_AF368036 51 MRV2/19/242/mouse/2019/Germany_MN639761 MRV1/466/bat/2017/USA_OP057379 using MEGA X software. 92 86 MRV2/5515-3/bat/2011/Italy_KU194672 100 MRV2/115/bat/2017/USA_OP037826 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900701 MRV3/SI-MRV01/human/2013/Slovenia_KF154731 100 MRV1/HB-A/mink/2013/China_KC462155 The numbers at nodes denote MRV1/WIV8/bat/2011/China_KT444568 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900702 99 100 99 70 MRV1/THK0617/wastewater/2020/Japan_LC613225 MRV2/RpMRV-YN2012/bat/2012/China_ KM087112 99 MRV1/WIV2/bat/2007/China_KT444528 MRV1 MRV3/342/bat/2008/Germany_ JQ412762 bootstrap values based on 1000 100 MRV1/B19-02/bat/2019/South Korea_MW582628 MRV2/809/bat/2017/USA_ OP057391 96 MRV1/HLJYC2017/swine/2017/China_MN788300 86 MRV2/Osaka1994/human/1994/Japan LC476902 MRV1/40/bat/2018/USA_ OP057400 replicates. The scale bar shows 100 MRV2/Osaka2014/human/2014/Japan_ LC476922 MRV1/466/bat/2017/USA_ OP057378 MRV4/Ndelle/mouse/1974/Cameroon_ AF368035 Avian orthoreovirus_HM222973 MRV4 MRV3/SD-14/mink/2014/China_KT224510 NelsonBay_AF059722 the evolutionary distance in 100 99 MRV3/WIV7/bat/2011/China_KT444558 MRV3/T3D/human/2002/USA_HM159619 0.50 96 MRV3/T3/206645-31/2011/Italy_JQ979275 terms of nucleotide substitu- MRV3 MRV3/342/bat/2008/Germany_JQ412761 MRV3/SI-MRV01/human/2013/Slovenia_KF154730 MRV3/Sl-MRV02/bat/2010/Slovenia_MG457084 tions per site. The virus strain NelsonBay_AF218360 Avian orthoreovirus_HM222974 Kj22-33 is shown in bold red. 0.50 Virus strains are labeled as S3 segment S4 segment MRV2/17-EF40/bat/2017/USA_MW718870 89 Kj22-33/bat/2022/Japan follows: MRV serotype/strain MRV2/809/bat/2017/USA_OP057392 MRV2/THK0325/wastewater/2020/Japan_LC613216 91 MRV3/SD-14/mink/2014/China_KT224512 MRV2/WIV3/bat/2011/China_ KT444581 MRV2/THK0325/wastewater/2020/Japan_LC613217 name/detection host or material/ MRV1/HLJYC2017/swine/2017/China_MN788303 MRV2/OV204/deer/2016/USA_MK092972 90 MRV1/B19-02/bat/2019/South Korea_MW582631 Kj22-33/bat/2022/Japan MRV1/THK0617/wastewater/2020/Japan_LC613226 detection year/country/GenBank MRV2/Osaka2014/human/2014/Japan_LC476923 81 MRV1/WIV2/bat/2007/China_KT444531 MRV2/Osaka1994/human/1994/Japan_LC476903 99 MRV2/WIV4/bat/2011/China_KT444541 MRV2/WIV4/bat/2011/China_KT444540 MRV2/Osaka2005/human/2005/Japan_LC476914 accession number. The four MRV2/Osaka2005/human/2005/Japan_LC476913 MRV2/OV204/deer/2016/USA_MK092973 MRV1/WIV2/bat/2007/China_KT444530 97 100 MRV3/SD-14/mink/2014/China_KT224513 99 MRV2/WIV3/bat/2011/China_KT444580 serotype groups are indicated MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900704 MRV1/HLJYC2017/swine/2017/China_MN788302 MRV2/809/bat/2017/USA_OP057393 78 MRV1/B19-02/bat/2019/South Korea_MW582630 98 MRV2/Osaka1994/human/1994/Japan_LC476904 MRV1/40/bat/2018/USA_OP057402 88 on the right-hand side of the S1 48 37 100 MRV1/466/bat/2017/USA_OP057380 99 MRV2/Osaka2014/human/2014/Japan_LC476924 MRV2/115/bat/2017/USA_OP037827 23 MRV2/17-EF40/bat/2017/USA_MW718871 MRV1/THK0617/wastewater/2020/Japan_LC613227 segment tree. 43 MRV1/40/bat/2018/USA_OP057403 MRV2/RpMRV-YN2012/bat/2012/China_KM087113 MRV4/Ndelle/mouse/1974/Cameroon_AF368037 MRV3/342/bat/2008/Germany_JQ412763 MRV2/RpMRV-YN2012/bat/2012/China_KM087114 MRV3/SI-MRV01/human/2013/Slovenia_KF154732 100 MRV3/342/bat/2008/Germany_JQ412764 NelsonBay_AF059726 99 MRV3/SI-MRV01/human/2013/Slovenia_KF154733 Avian orthoreovirus_HM222972 MRV1/466/bat/2017/USA_OP057381 100MRV2/115/bat/2017/USA_OP037828 0.50 NelsonBay_NC038658 Avian orthoreovirus_HM222971 0.50 M1 segment M2 segment 100 MRV2/17-EF40/bat/2017/USA_MW718868 88 MRV1/HLJYC2017/swine/2017/China_MN788298 MRV2/809/bat/2017/USA_ OP057394 MRV2/THK0325/wastewater/2020/Japan_LC613213 99 100 MRV2/809/bat/2017/USA_ OP057395 MRV3/SD-14/mink/2014/China_KT224507 54 MRV2/OV204/deer/2016/USA_MK092968 MRV2/Osaka2005/human/2005/Japan_LC476908 81 85 MRV3/SD-14/mink/2014/China_KT224508 MRV2/Osaka1994/human/1994/Japan_LC476898 MRV2/WIV4/bat/2011/China_ KT444536 98 MRV2/WIV4/bat/2011/China_ KT444535 MRV2/Osaka2014/human/2014/Japan_ LC476919 MRV2/Osaka2014/human/2014/Japan_ LC476918 86 81 MRV2/Osaka1994/human/1994/Japan_ LC476899 MRV2/THK0325/wastewater/2020/Japan_LC613212 79 MRV2/Osaka2005/human/2005/Japan_ LC476909 MRV1/THK0617/wastewater/2020/Japan_LC613222 93 77 MRV2/RpMRV-YN2012/bat/2012/China_ KM087109 MRV2/RpMRV-YN2012/bat/2012/China_KM087108 MRV3/342/bat/2008/Germany_ JQ412757 MRV1/WIV2/bat/2007/China_KT444525 85 MRV3/SI-MRV01/human/2013/Slovenia_KF154728 MRV2/WIV3/bat/2011/China_ KT444575 60 MRV1/40/bat/2018/USA_ OP057405 94 MRV1/WIV2/bat/2007/China_ KT444526 99 MRV1/HLJYC2017/swine/2017/China_MN788297 MRV2/WIV3/bat/2011/China_ KT444576 64 MRV1/466/bat/2017/USA_OP057382 MRV1/BatMRV1-IT2011/bat/2011/Italy_ KT900699 100 MRV2/115/bat/2017/USA_OP037829 75 MRV4/Ndelle/mouse/1974/Cameroon_ AF368034 MRV1/40/bat/2018/USA_ OP057404 100 MRV2/17-EF40/bat/2017/USA_MW718866 100 56 Kj22-33/bat/2022/Japan MRV1/THK0617/wastewater/2020/Japan_LC613223 98 MRV1/B19-02/bat/2019/South Korea_ MW582625 Kj22-33/bat/2022/Japan MRV2/OV204/deer/2016/USA_MK092967 99 MRV1/B19-02/bat/2019/South Korea_ MW582626 MRV1/BatMRV1-IT2011/bat/2011/Italy_ KT900698 MRV2/115/bat/2017/USA_OP037830 MRV3/342/bat/2008/Germany_ JQ412758 100 MRV1/466/bat/2017/USA_ OP057383 95 MRV3/SI-MRV01/human/2013/Slovenia_KF154727 NelsonBay_LC619333 Avian orthoreovirus_HM222976 Avian orthoreovirus_HM222977 NelsonBay_LC619332 0.10 0.20 M3 segment L1 segment MRV2/WIV3/bat/2011/China_ KT444577 MRV2/17-EF40/bat/2017/USA_MW718862 MRV2/809/bat/2017/USA_OP57397 86 MRV2/OV204/deer/2016/USA_MK092969 MRV2/THK0325/wastewater/2020/Japan_LC613209 Kj22-33/bat/2022/Japan 89 Kj22-33/bat/2022/Japan MRV1/HLJYC2017/swine/2017/China_MN788299 99 MRV2/OV204/deer/2016/USA_MK092964 MRV3/SD-14/mink/2014/China_KT224509 MRV3/SD-14/mink/2014/China_KT224504 MRV2/17-EF40/bat/2017/USA_ MW718867 MRV2/WIV4/bat/2011/China_KT444532 MRV2/THK0325/wastewater/2020/Japan_LC613214 MRV1/THK0617/wastewater/2020/Japan_LC613219 MRV2/WIV4/bat/2011/China_ KT444537 MRV2/Osaka2005/human/2005/Japan_LC476905 MRV2/809/bat/2017/USA_ OP057396 97 MRV2/Osaka1994/human/1994/Japan_LC476895 MRV2/Osaka2005/human/2005/Japan_ LC476910 95 99 MRV2/Osaka2014/human/2014/Japan_LC476915 97 MRV1/WIV2/bat/2007/China_KT444537 MRV1/B19-02/bat/2019/South Korea_MW58262 MRV1/THK0617/wastewater/2020/Japan MRV1/466/bat/2017/USA_OP057385 96 MRV1/B19-02/bat/2019/South Korea_ MW582627 MRV2/115/bat/2017/USA_OP037832 MRV1/40/bat/2018/USA_ OP057406 MRV2/RpMRV-YN2012/bat/2012/China_KM087105 MRV1/BatMRV1-IT2011/bat/2011/Italy_ KT900700 MRV4/Ndelle/mouse/1974/Cameroon_AF368033 1 MRV2/RpMRV-YN2012/bat/2012/China_ KM087110 MRV1/40/bat/2018/USA_OP057407 99 MRV3/342/bat/2008/Germany_ JQ412760 38 100 MRV3/342/bat/2008/Germany_ JQ412755 MRV3/SI-MRV01/human/2013/Slovenia_ KF154729 MRV3/SI-MRV01/human/2013/Slovenia_KF154724 54 MRV1/466/bat/2017/USA_OP057384 100 100 MRV1/WIV2/bat/2007/China_KT444522 MRV2/115/bat/2017/USA_ OP037831 MRV2/WIV3/bat/2011/China_KT444572 MRV2/Osaka2014/human/2014/Japan_ LC476920 MRV1/HLJYC2017/swine/2017/China_MN788294 MRV2/Osaka1994/human/1994/Japan_ LC476900 NelsonBay_LC619329 NelsonBay_LC619334 Avian orthoreovirus_HM22978 Avian orthoreovirus_HM222975 0.20 0.20 L2 segment L3 segment 99 Kj22-33/bat/2022/Japan Kj22-33/bat/2022/Japan 99 MRV2/WIV4/bat/2011/China_KT444533 MRV2/OV204/deer/2016/USA_MK092966 MRV2/Osaka2005/human/2005/Japan_LC476906 MRV2/17-EF40/bat/2017/USA_MW718864 100 97 MRV1/HB-A/mink/2013/China_KC462150 MRV2/809/bat/2017/USA_OP057399 MRV2/Osaka1994/human/1994/Japan_LC47896 MRV1/HLJYC2017/swine/2017/China_MN788296 MRV2/Osaka2014/human/2014/Japan_LC476916 99 MRV2/Osaka2005/human/2005/JapanLC476907 98 MRV2/WIV3/bat/2011/China_KT444573 MRV1/WIV2/bat/2007/China_KT444524 MRV1/HLJYC2017/swine/2017/China_MN788295 MRV3/SD-14/mink/2014/China_KT224506 MRV1/WIV2/bat/2007/China_KT444523 MRV2/Osaka2014/human/2014/Japan_LC476917 MRV1/THK0617/wastewater/2020/Japan_LC613220 81 MRV1/HB-A/mink/2013/China_KC462151 99 MRV2/17-EF40/bat/2017/USA_MW718863 97 MRV2/WIV3/bat/2011/China_KT444574 87 MRV2/bat/2017/USA_OP057398 MRV2/THK0325/wastewater/2020/Japan_LC613211 MRV2/19/242/mouse/2019/Germany_MN639756 100 98 MRV2/WIV4/bat/2011/China_KT444534 MRV2/THK0325/wastewater/2020/Japan_LC613210 100 98 MRV2/Osaka1994/human/1994/Japan_ LC476897 MRV2/OV204/deer/2016/USA_MK092965 67 99 MRV1/THK0617/wastewater/2020/Japan_LC613221 100 MRV3/SD-14/mink/2014/China_KT224505 MRV1/40/bat/2018/USA_OP057409 MRV2/115/bat/2017/USA_OP037833 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900697 100 MRV1/40/bat/2018/USA_OP057408 100 MRV1/466/bat/2017/USA_OP057387 MRV1/466/bat/2017/USA_OP057386 95 MRV2/115/bat/2017/USA_OP037834 MRV2/RpMRV-YN2012/bat/2012/China_KM087106 MRV1/B19-02/bat/2019/South Korea_MW582624 80 MRV1/B19-02/bat/2019/South Korea_MW582623 MRV2/RpMRV-YN2012/bat/2012/China_KM087107 97 MRV1/BatMRV1-IT2011/bat/2011/Italy_KT900696 MRV3/342/bat/2008/Germany_JQ412755 99 100 MRV3/342/bat/2008/Germany_JQ412756 MRV3/SI-MRV01/human/2013/Slovenia_KF154726 MRV3/SI-MRV01/human/2013/Slovenia_KF154725 NelsonBay_LC619331 NelsonBay_LC619330 Avian orthoreovirus_HM222979 Avian orthoreovirus_HM222980 0.20 0.20 1 3 165 Page 4 of 5 A. 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