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16.09.2022 | Original Article

Genetic diversity, reassortment, and recombination of mammalian orthoreoviruses from Japanese porcine fecal samples

verfasst von: Yuka Fukase, Fujiko Minami, Tsuneyuki Masuda, Toru Oi, Hitoshi Takemae, Hiroho Ishida, Hironobu Murakami, Naoyuki Aihara, Takanori Shiga, Junichi Kamiie, Tetsuya Furuya, Tetsuya Mizutani, Mami Oba, Makoto Nagai

Erschienen in: Archives of Virology | Ausgabe 12/2022

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Abstract

Mammalian orthoreoviruses (MRVs) are non-enveloped double-stranded RNA viruses with a broad host range. MRVs are prevalent worldwide, and in Japan, they have been isolated from various hosts, including humans, dogs, cats, wild boars, and pigs, and they have also been found in sewage. However, Japanese porcine MRVs have not been genetically characterized. While investigating porcine enteric viruses including MRV, five MRVs were isolated from the feces of Japanese pigs using MA104 cell culture. Genetic analysis of the S1 gene revealed that the Japanese porcine MRV isolates could be classified as MRV-2 and MRV-3. Whole genome analysis showed that Japanese porcine MRVs exhibited genetic diversity, although they shared sequence similarity with porcine MRV sequences in the DDBJ/EMBL/GenBank database. Several potential intragenetic reassortment events were detected among MRV strains from pigs, sewage, and humans in Japan, suggesting zoonotic transmission. Furthermore, homologous recombination events were identified in the M1 and S1 genes of Japanese porcine MRV. These findings imply that different strains of Japanese porcine MRV share a porcine MRV genomic backbone and have evolved through intragenetic reassortment and homologous recombination events.

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Day JM (2009) The diversity of the orthoreoviruses: molecular taxonomy and phylogenetic divides. Infect Genet Evol 9:390–400. https://doi.org/10.1016/j.meegid.2009.01.011CrossRef

Guglielmi KM, Johnson EM, Stehle T, Dermody TS (2006) Attachment and cell entry of mammalian orthoreovirus. Curr Top Microbiol Immunol 309:1–38. https://doi.org/10.1007/3-540-30773-7_1CrossRef

Tai JH, Williams JV, Edwards KM, Wright PF, Crowe JE Jr, Dermody TS (2005) Prevalence of reovirus-specific antibodies in young children in Nashville, Tennessee. J Infect Dis 191:1221–1224. https://doi.org/10.1086/428911CrossRef

Yamamoto SP, Motooka D, Egawa K, Kaida A, Hirai Y, Kubo H, Motomura K, Nakamura S, Iritani N (2020) Novel human reovirus isolated from children and its long-term circulation with reassortments. Sci Rep 10(1):963. https://doi.org/10.1038/s41598-020-58003-9CrossRef

Johansson PJ, Sveger T, Ahlfors K, Ekstrand J, Svensson L (1996) Reovirus type 1 associated with meningitis. Scand J Infect Dis 28:117–120. https://doi.org/10.3109/00365549609049060CrossRef

Hermann L, Embree J, Hazelton P, Wells B, Coombs RT (2004) Reovirus type 2 isolated from cerebrospinal fluid. Pediatr Infect Dis J 23:373–375. https://doi.org/10.1097/00006454-200404000-00026CrossRef

Tyler KL, Barton ES, Ibach ML, Robinson C, Campbell JA, O’Donnell SM, Valyi-Nagy T, Clarke P, Wetzel JD, Dermody T (2004) Isolation and molecular characterization of a novel type 3 reovirus from a child with meningitis. J Infect Dis 189:1664–1675. https://doi.org/10.1086/383129CrossRef

Chua KB, Crameri G, Hyatt A, Yu M, Tompang MR, Rosli J, McEachern J, Crameri S, Kumarasamy V, Eaton BT, Wang LF (2007) A previously unknown reovirus of bat origin is associated with an acute respiratory disease in humans. Proc Natl Acad Sci USA 104:11424–11429. https://doi.org/10.1073/pnas.0701372104CrossRef

Cheng P, Lau CS, Lai A, Ho E, Leung P, Chan F, Wong A, Lim W (2009) A novel reovirus isolated from a patient with acute respiratory disease. J Clin Virol 45:79–80. https://doi.org/10.1016/j.jcv.2009.03.001CrossRef

10.

Chua KB, Voon K, Yu M, Keniscope C, Abdul Rasid K, Wang LF (2011) Investigation of a potential zoonotic transmission of orthoreovirus associated with acute influenza-like illness in an adult patient. PLoS ONE 6(10):e25434. https://doi.org/10.1371/journal.pone.0025434CrossRef

11.

Kwon HJ, Kim HH, Kim HJ, Park JG, Son KY, Jung J, Lee WS, Cho KO, Park SJ, Kang MI (2012) Detection and molecular characterization of porcine type 3 orthoreoviruses circulating in South Korea. Vet Microbiol 157:456–463. https://doi.org/10.1016/j.vetmic.2011.12.032CrossRef

12.

Thimmasandra Narayanappa A, Sooryanarain H, Deventhiran J, Cao D, Ammayappan Venkatachalam B, Kambiranda D, LeRoith T, Heffron CL, Lindstrom N, Hall K, Jobst P, Sexton C, Meng XJ, Elankumaran S (2015) A novel pathogenic mammalian orthoreovirus from diarrheic pigs and swine blood meal in the United States. MBio. https://doi.org/10.1128/mBio.00593-15,e00593-e00515CrossRef

13.

Lelli D, Beato MS, Cavicchio L, Lavazza A, Chiapponi C, Leopardi S, Baioni L, De Benedictis P, Moreno A (2016) First identification of mammalian orthoreovirus type 3 in diarrheic pigs in Europe. Virol J 13:139. https://doi.org/10.1186/s12985-016-0593-4CrossRef

14.

Qin P, Li H, Wang JW, Wang B, Xie RH, Xu H, Zhao LY, Li L, Pan Y, Song Y, Huang YW (2017) Genetic and pathogenic characterization of a novel reassortant mammalian Orthoreovirus 3 (MRV3) from a diarrheic piglet and seroepidemiological survey of MRV3 in diarrheic pigs from east China. Vet Microbiol 208:126–136. https://doi.org/10.1016/j.vetmic.2017.07.021CrossRef

15.

Luo Y, Fei L, Yue H, Li S, Ma H, Tang C (2020) Prevalence and genomic characteristics of a novel reassortment mammalian orthoreovirus type 2 in diarrhea piglets in Sichuan, China. Infect Genet Evol 85:104420. https://doi.org/10.1016/j.meegid.2020.104420,104420CrossRef

16.

Wang L, Li Y, Walsh T, Shen Z, Li Y, Deb Nath N, Lee J, Zheng B, Tao Y, Paden CR, Queen K, Zhang S, Tong S, Ma W (2021) Isolation and characterization of novel reassortant mammalian orthoreovirus from pigs in the United States. Emerg Microbes Infect 10:1137–1147. https://doi.org/10.1080/22221751.2021.1933608CrossRef

17.

Dermody TS, Parker JSL, Sherry B (2013) Orthoreoviruses. In: David MK, Peter MH (eds) Fields virology. Lippincott Williams & Wilkins, Philadelphia, pp 1304–1346

18.

Hirahara T, Yasuhara H, Matsui O, Kodama K, Nakai M, Sasaki N (1988) Characteristics of reovirus type 1 from the respiratory tract of pigs in Japan. Nihon Juigaku Zasshi. 50:353–361. https://doi.org/10.1292/jvms1939.50.353CrossRef

19.

Fukutomi T, Sanekata T, Akashi H (1996) Isolation of reovirus type 2 from diarrheal feces of pigs. J Vet Med Sci 58:555–557. https://doi.org/10.1292/jvms.58.555CrossRef

20.

Zhang W, Kataoka M, Doan YH, Oi T, Furuya T, Oba M, Mizutani T, Oka T, Li TC, Nagai M (2021) Isolation and characterization of mammalian orthoreovirus type 3 from a fecal sample from a wild boar in Japan. Arch Virol 166:1671–1680. https://doi.org/10.1007/s00705-021-05053-7CrossRef

21.

Leary TP, Erker JC, Chalmers ML, Cruz AT, Wetzel JD, Desai SM, Mushahwar IK, Dermody TS (2002) Detection of mammalian reovirus RNA by using reverse transcription-PCR: sequence diversity within the lambda3-encoding L1 gene. J Clin Microbiol 40:1368–1375. https://doi.org/10.1128/JCM.40.4.1368-1375.2002CrossRef

22.

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876CrossRef

23.

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054CrossRef

24.

Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

25.

Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1(1):vev003. https://doi.org/10.1093/ve/vev003CrossRef

26.

Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160. https://doi.org/10.1128/JVI.73.1.152-160.1999CrossRef

27.

Farkas SL, Marton S, Dandar E, Kugler R, Gal B, Jakab F, Balint A, Kecskemeti S, Banyai K (2016) Lineage diversification, homo- and heterologous reassortment and recombination shape the evolution of chicken orthoreoviruses. Sci Rep 10(6):36960. https://doi.org/10.1038/srep36960CrossRef

28.

Noh JY, Lee DH, Lim TH, Lee JH, Day JM, Song CS (2018) Isolation and genomic characterization of a novel avian orthoreovirus strain in Korea, 2014. Arch Virol 163:1307–1316. https://doi.org/10.1007/s00705-017-3667-8CrossRef

29.

Ye D, Ji Z, Shi H, Chen J, Shi D, Cao L, Liu J, Li M, Dong H, Jing Z, Wang X, Liu Q, Fan Q, Cong G, Zhang J, Han Y, Zhou J, Gu J, Zhang X, Feng L (2020) Molecular characterization of an emerging reassortant mammalian orthoreovirus in China. Arch Virol 165:2367–2372. https://doi.org/10.1007/s00705-020-04712-5CrossRef

30.

Kitamura K, Takagi H, Oka T, Kataoka M, Ueki Y, Sakagami A (2021) Intertypic reassortment of mammalian orthoreovirus identified in wastewater in Japan. Sci Rep 11(1):12583. https://doi.org/10.1038/s41598-021-92019-zCrossRef

31.

Yang XL, Tan B, Wang B, Li W, Wang N, Luo CM, Wang MN, Zhang W, Li B, Peng C, Ge XY, Zhang LB, Shi ZL (2015) Isolation and identification of bat viruses closely related to human, porcine and mink orthoreoviruses. J Gen Virol 96:3525–3531. https://doi.org/10.1099/jgv.0.000314CrossRef

32.

Cavicchio L, Tassoni L, Zamperin G, Campalto M, Carrino M, Leopardi S, Benedictis P, Beato MS (2020) Unexpected genetic diversity of two novel swine MRVs in Italy. Viruses 12(5):574. https://doi.org/10.3390/v12050574CrossRef

33.

Harima H, Sasaki M, Kajihara M, Gonzalez G, Simulundu E, Bwalya EC, Qiu Y, Okuya K, Isono M, Orba Y, Takada A, Hang’ombe BM, Mweene AS, Sawa H (2020) Characterization of mammalian orthoreoviruses isolated from feces of pigs in Zambia. J Gen Virol 101:1027–1036. https://doi.org/10.1099/jgv.0.001476CrossRef

34.

Zhang C, Liu L, Wang P, Liu S, Lin W, Hu F, Wu W, Chen W, Cui S (2011) A potentially novel reovirus isolated from swine in northeastern China in 2007. Virus Genes 43:342–349. https://doi.org/10.1007/s11262-011-0642-4CrossRef

35.

Zhang W, Kataoka M, Doan HY, Wu FT, Haga K, Takeda N, Muramatsu M, Li TC (2020) Isolation and characterization of mammalian orthoreoviruses using a cell line resistant to Sapelovirus infection. Transbound Emerg Dis 67:2849–2859. https://doi.org/10.1111/tbed.13655CrossRef

36.

Castilla D, Escobar V, Ynga S, Llanco L, Manchego A, Lázaro C, Navarro D, Santos N, Rojas M (2021) Enteric viral infections among Domesticated South American Camelids: First detection of mammalian orthoreovirus in camelids. Animals (Basel) 11(5):1455. https://doi.org/10.3390/ani11051455CrossRef

37.

Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gomara M, Maes P, Patton JT, Rahman M, Van Ranst M (2008) Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82:3204–3219. https://doi.org/10.1128/JVI.02257-07CrossRef

38.

Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Banyai K, Brister JR, Buesa J, Esona MD, Estes MK, Gentsch JR, Iturriza-Gomara M, Johne R, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Parreno V, Rahman M, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Patton JT, Desselberger U, Van Ranst M (2011) Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397–1413. https://doi.org/10.1007/s00705-011-1006-zCrossRef

39.

Kokubu T, Takahashi T, Takamura K, Yasuda H, Hiramatsu K, Nakai M (1993) Isolation of reovirus type 3 from dogs with diarrhea. J Vet Med Sci 55:453–454. https://doi.org/10.1292/jvms.55.453CrossRef

40.

Meng XJ, Lindsay DS, Sriranganathan N (2009) Wild boars as sources for infectious diseases in livestock and humans. Philos Trans R Soc Lond B Biol Sci 364:2697–2707. https://doi.org/10.1098/rstb.2009.0086CrossRef

41.

Ohdachi S, Ishibashi Y, Iwasa MA, Saitoh T (eds) (2009) The wild mammals of Japan. Shoukadoh Book Sellers, Kyoto, p 544

42.

Postel A, Nishi T, Kameyama KI, Meyer D, Suckstorff O, Fukai K, Becher P (2019) Reemergence of classical swine fever. Japan, Emerg Infect Dis 25:1228–1231. https://doi.org/10.3201/eid2506.181578CrossRef

43.

Yamazaki Y, Adachi F, Sawamura A (2016) Multiple origins and admixture of recently expanding Japanese wild boar (Sus scrofa leucomystax) populations in Toyama Prefecture of Japan. Zool Sci 33:38–43. https://doi.org/10.2108/zs150092CrossRef

44.

Hoxie I (2020) Dennehy JJ (2020) Intragenic recombination influences rotavirus diversity and evolution. Virus Evol 6(1):vez059. https://doi.org/10.1093/ve/vez059CrossRef

45.

Cao D, Barro M, Hoshino Y (2008) Porcine rotavirus bearing an aberrant gene stemming from an intergenic recombination of the NSP2 and NSP5 genes is defective and interfering. J Virol 82:6073–6077. https://doi.org/10.1128/JVI.00121-08CrossRef

46.

Oki H, Masuda T, Hayashi-Miyamoto M, Kawai M, Ito M, Madarame H, Fukase Y, Takemae H, Sakaguchi S, Furuya T, Mizutani T, Oba M, Nagai M (2022) Genomic diversity and intragenic recombination of species C rotaviruses. J Gen Virol. https://doi.org/10.1099/jgv.0.001703CrossRef

47.

Smith SC, Gribble J, Diller JR, Wiebe MA, Thoner TW Jr, Denison MR, Ogden KM (2021) Reovirus RNA recombination is sequence directed and generates internally deleted defective genome segments during passage. J Virol 95(8):e02181-e2220. https://doi.org/10.1128/JVI.02181-20CrossRef

Titel: Genetic diversity, reassortment, and recombination of mammalian orthoreoviruses from Japanese porcine fecal samples
verfasst von: Yuka Fukase
Fujiko Minami
Tsuneyuki Masuda
Toru Oi
Hitoshi Takemae
Hiroho Ishida
Hironobu Murakami
Naoyuki Aihara
Takanori Shiga
Junichi Kamiie
Tetsuya Furuya
Tetsuya Mizutani
Mami Oba
Makoto Nagai
Publikationsdatum: 16.09.2022
Verlag: Springer Vienna
Erschienen in: Archives of Virology / Ausgabe 12/2022
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-022-05602-8

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