Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. 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.2009.01.011

    Article  CAS  Google Scholar 

  2. 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_1

    Article  CAS  Google Scholar 

  3. 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/10.1086/428911

    Article  Google Scholar 

  4. 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/s41598-020-58003-9

    Article  CAS  Google Scholar 

  5. 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/10.3109/00365549609049060

    Article  CAS  Google Scholar 

  6. 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/10.1097/00006454-200404000-00026

    Article  Google Scholar 

  7. 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/10.1086/383129

    Article  CAS  Google Scholar 

  8. 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.0701372104

    Article  CAS  Google Scholar 

  9. 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.2009.03.001

    Article  Google Scholar 

  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.0025434

    Article  CAS  Google Scholar 

  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.2011.12.032

    Article  Google Scholar 

  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-e00515

    Article  Google Scholar 

  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/s12985-016-0593-4

    Article  Google Scholar 

  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.2017.07.021

    Article  CAS  Google Scholar 

  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.2020.104420,104420

    Article  CAS  Google Scholar 

  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/10.1080/22221751.2021.1933608

    Article  CAS  Google Scholar 

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

    Google Scholar 

  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/jvms1939.50.353

    Article  CAS  Google Scholar 

  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.58.555

    Article  CAS  Google Scholar 

  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/s00705-021-05053-7

    Article  CAS  Google Scholar 

  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.40.4.1368-1375.2002

    Article  CAS  Google Scholar 

  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/25.24.4876

    Article  CAS  Google Scholar 

  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/msw054

    Article  CAS  Google Scholar 

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

    Google Scholar 

  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/vev003

    Article  Google Scholar 

  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.73.1.152-160.1999

    Article  CAS  Google Scholar 

  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/srep36960

    Article  CAS  Google Scholar 

  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/s00705-017-3667-8

    Article  CAS  Google Scholar 

  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/s00705-020-04712-5

    Article  CAS  Google Scholar 

  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-z

    Article  CAS  Google Scholar 

  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.0.000314

    Article  CAS  Google Scholar 

  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/v12050574

    Article  CAS  Google Scholar 

  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.0.001476

    Article  CAS  Google Scholar 

  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/s11262-011-0642-4

    Article  CAS  Google Scholar 

  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.13655

    Article  CAS  Google Scholar 

  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/ani11051455

    Article  Google Scholar 

  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.02257-07

    Article  CAS  Google Scholar 

  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-z

    Article  CAS  Google Scholar 

  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.55.453

    Article  CAS  Google Scholar 

  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.2009.0086

    Article  CAS  Google Scholar 

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

    Google Scholar 

  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/eid2506.181578

    Article  Google Scholar 

  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/zs150092

    Article  Google Scholar 

  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/vez059

    Article  Google Scholar 

  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.00121-08

    Article  CAS  Google Scholar 

  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.0.001703

    Article  Google Scholar 

  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.02181-20

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the JSPS KAKENHI (Grant numbers 18K05977 and 21K05947).

Author information

Authors and Affiliations

  1. School of Veterinary Medicine, Azabu University, Sagamihara, Kanagawa, 252-5201, Japan

    Yuka Fukase, Hiroho Ishida, Hironobu Murakami, Naoyuki Aihara, Takanori Shiga, Junichi Kamiie, Mami Oba & Makoto Nagai

  2. Ishikawa Hokubu Livestock Hygiene Service Center, Nanao, Ishikawa, 929-2121, Japan

    Fujiko Minami

  3. Seibu Livestock Hygiene Service Center, Houki, Tottori, 689-4213, Japan

    Tsuneyuki Masuda

  4. Faculty of Bioresources and Environmental Science, Ishikawa Prefectural University, Nonoichi, Ishikawa, 921-8836, Japan

    Toru Oi

  5. Center for Infectious Disease Epidemiology and Prevention Research, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Hitoshi Takemae, Tetsuya Mizutani, Mami Oba & Makoto Nagai

  6. Cooperative Department of Veterinary Medicine, Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Tetsuya Furuya

Authors
  1. Yuka Fukase
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fujiko Minami
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tsuneyuki Masuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Toru Oi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hitoshi Takemae
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroho Ishida
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hironobu Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Naoyuki Aihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Takanori Shiga
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Junichi Kamiie
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Tetsuya Furuya
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Tetsuya Mizutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Mami Oba
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Makoto Nagai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mami Oba or Makoto Nagai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Research involving human participants and/or animals

This study did not involve any human participants and animals.

Additional information

Handling Editor: Zhenhai Chen.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Fig. S1

Phylogenetic analysis based on nearly complete L1 (A), L2 (B), L3 (C), M1 (D), M2 (E), M3 (F), S1 (G), S2 (H), S3 (I), and S4 (J) gene nucleotide sequences of Japanese porcine MRVs and MRV strains obtained from the DDBJ/EMBL/GenBank databases. The phylogenetic trees were constructed using the maximum-likelihood method in MEGA7 with best-fit models (the GTR+G+I model for the L1, L2, L3, M1, M2, M3, S2, and S3 phylogenetic trees and the GTR+G model for the S1 and S4 phylogenetic trees). Bootstrap values above 70 (1,000 replicates) are shown. The bars represent the corrected genetic distances. Japanese porcine MRVs and Japanese MRVs from humans, wild boar, lion, and sewage are indicated in red and blue, respectively. (PDF 408 KB)

Supplementary Fig. S2

(A-a) Recombination analysis of the L3 gene segment of Bat/WIV3/CHN vs. Deer/OV204/USA (yellow curve), Bat/WIV3/CHN vs. Bat/WIV5/CHN (blue-green curve), and Deer/OV204/USA vs. Bat/WIV5/CHN (purple curve). (A-b) Similarity plots of Bat/WIV3/CHN (blue-green curve) and Deer/OV204/USA (purple curve), and Bat/WIV5/CHN as a query sequence, with a sliding window of 200 nucleotides and a moving step size of 20 nucleotides. (B-a) Recombination analysis of the L3 gene segment of Pig/4560-3/USA vs. Pig/4560-1/USA (yellow curve), Pig/4560-3/USA vs. Pig/4560-2/USA (blue-green curve), and Pig/4560-1/USA vs. Pig/4560-2/USA (purple curve). (B-b) Similarity plots of Pig/4560-3/USA (yellow curve) and Pig/4560-2/USA (purple curve), and Pig/4560-1/USA as a query sequence, with a sliding window of 200 nucleotides and a moving step size of 20 nucleotides. (C-a) Recombination analysis of the M2 gene segment of Bat/WIV4/CHN vs. Bat/WIV3/CHN (yellow curve), Bat/WIV4/CHN vs. Bat/WIV5/CHN (blue-green curve), and Bat/WIV3/CHN vs. Bat/WIV5/CHN (purple curve). (C-b) Similarity plots of Bat/WIV3/CHN (blue-green curve) and Bat/WIV4/CHN (purple curve), and Bat/WIV5/CHN as a query sequence, with a sliding window of 200 nucleotides and a moving step size of 20 nucleotides. (D-a) Recombination analysis of the M2 gene segment of Pig/HLJ/CHN vs. Human/SI-MRV01/SVN (yellow curve), Pig/HLJ/CHN vs. Bat/RpMRV-YN2012/CHN (blue-green curve), and Human/SI-MRV01/SVN vs. Bat/RpMRV-YN2012/CHN (purple curve). (D-b) Similarity plots of Pig/HLJ/CHN (yellow curve) and Bat/RpMRV-YN2012/CHN (purple curve), and Human/SI-MRV01/SVN as a query sequence, with a sliding window of 200 nucleotides and a moving step size of 20 nucleotides (PDF 159 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fukase, Y., Minami, F., Masuda, T. et al. Genetic diversity, reassortment, and recombination of mammalian orthoreoviruses from Japanese porcine fecal samples. Arch Virol 167, 2643–2652 (2022). https://doi.org/10.1007/s00705-022-05602-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05602-8

Search

Navigation