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Virus Genes

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Complete genomic analysis and molecular characterization of Japanese porcine sapeloviruses

  • Fujiko Sunaga
  • Tsuneyuki Masuda
  • Mika Ito
  • Masataka Akagami
  • Yuki Naoi
  • Kaori Sano
  • Yukie Katayama
  • Tsutomu Omatsu
  • Mami Oba
  • Shoichi Sakaguchi
  • Tetsuya Furuya
  • Hiroshi Yamasato
  • Yoshinao Ouchi
  • Junsuke Shirai
  • Tetsuya Mizutani
  • Makoto NagaiEmail author
Article
  • 55 Downloads

Abstract

The Porcine Sapelovirus (PSV) is an enteric virus of pigs that can cause various disorders. However, there are few reports that describe the molecular characteristics of the PSV genome. In this study, almost the entire genomes of 23 PSVs detected in Japanese pigs were analyzed using bioinformatics. Analysis of the cis-active RNA elements showed that the predicted secondary structures of the internal ribosome entry site in the 5′ untranslated region (UTR) and a cis-replication element in the 2C coding region were conserved among PSVs. In contrast, those at the 3′ UTR were different for different PSVs; however, tertiary structures between domains were conserved across all PSVs. Phylogenetic analysis of nucleotide sequences of the complete VP1 region showed that PSVs exhibited sequence diversity; however, they could not be grouped into genotypes due to the low bootstrap support of clusters. The insertion and/or deletion patterns in the C-terminal VP1 region were not related to the topology of the VP1 tree. The 3CD phylogenetic tree was topologically different from the VP1 tree, and PSVs from the same country were clustered independently. Recombination analysis revealed that recombination events were found upstream of the P2 region and some recombination breakpoints involved insertions and/or deletions in the C-terminal VP1 region. These findings demonstrate that PSVs show genetic diversity and frequent recombination events, particularly in the region upstream of the P2 region; however, PSVs could currently not be classified into genotypes and conserved genetic structural features of the cis-active RNA elements are observed across all PSVs.

Keywords

Complete genome analysis Japan Molecularly characterization Porcine feces Sapelovirus A 

Notes

Acknowledgements

This work was supported by JSPS KAKENHI, via Grants 15K07718 and 18K05977.

Author contributions

FS, TM, MI, MA, YN, KS, YK, TO, MO, SS, TF, HY, YO, JS, TM, MN TM, and MN conceived of the study. FS, TF, JS, TM, and MN designed the study. TM, MI, MA, HY, and YO collected samples from pigs and carried out RT-PCR. YN, KS, YK, TO, MO, and SS analyzed data using bioinformatics. FS, KS, SS, TF, JS, TM, and MN wrote the paper. All authors approved the submitted manuscript.

Compliance with ethical standards

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.

Informed consent

Not applicable.

Supplementary material

11262_2019_1640_MOESM1_ESM.xlsx (40 kb)
Supplementary Fig. 1. Sequence read depth of the contigs generated from the de novo sequence assembly. Mapping reads were conducted with regard to the contig using the CLC Genomics Workbench with the strictest parameter settings (mismatch cost, 2; insertion cost, 3; deletion cost, 3; length function, 0.9; and similarity function, 0.9) (XLSX 40 KB)
11262_2019_1640_MOESM2_ESM.xlsx (37 kb)
Supplementary Fig. 2. Genome analysis of the 5′ UTR at the nucleotide positions 169–443 in PSV V13/1957/GBR (Accession No. NC_003987), corresponding to that of IRES stem-loop domains II and III of Japanese PSVs using PSVs from the DDBJ/EMBL/GenBank database. a Alignment of nt sequences of the 5′ UTR (nucleotide position 169–443 of PSV V13/1957/GBR) of PSVs. b Secondary structure prediction of the IRES within the 5′ UTR of PSVs. The core domains II and III are shown (XLSX 36 KB)
11262_2019_1640_MOESM3_ESM.pptx (14.4 mb)
Supplementary Fig. 3. a Genome structure of PSV. be Similarity plots of the entire genomes of Japanese PSVs, constructed using a sliding window of 200 nt and a moving step size of 20 nt (upper). Recombination breakpoint analysis of Japanese PSVs (lower). Recombination breakpoints are indicated using black arrows (PPTX 14711 KB)
11262_2019_1640_MOESM4_ESM.pptx (4.4 mb)
Supplementary Fig. 4. A phylogenetic tree constructed based on the nt sequences from the complete P1 region of 23 PSVs detected in this study, using 52 PSV sequences from the DDBJ/EMBL/GenBank database. The phylogenetic tree was constructed by the maximum likelihood method using MEGA7, and bootstrap values (1000 replicates) > 70 are shown. The bar represents a corrected genetic distance. ● Denotes PSVs detected in the present study. PSVs detected in Japan, China, South Korea, the USA, German, France, the UK, and India are shows in red, blue, yellow, green, black, light green, purple, and brown, respectively (PPTX 4548 KB)
11262_2019_1640_MOESM5_ESM.pptx (4 mb)
Supplementary Table 1 Pairwise nucleotide sequence identities of the VP1 region (lower left) and 3CD region (upper right) between porcine sapeloviruses; the VP1 and 3CD regions, which showed sequence identities of ≥ 82.5% and ≥ 91.5%, are shown in yellow and red colors, respectively (PPTX 4089 KB)
11262_2019_1640_MOESM6_ESM.pptx (54 kb)
Supplementary Table 2 Pairwise amino acid sequence identities of the VP1 region (lower left) and 3CD region (upper right) between porcine sapeloviruses. The VP1 and 3CD regions, which showed sequence identities of ≥ 89.0% and ≥ 98.8%, are presented in yellow and red, respectively (PPTX 54 KB)

References

  1. 1.
    Abe M, Ito N, Sakai K, Kaku Y, Oba M, Nishimura M, Kurane I, Saijo M, Morikawa S, Sugiyama M, Mizutani T (2011) A novel sapelovirus-like virus isolation from wild boar. Virus Genes 43:243–248CrossRefGoogle Scholar
  2. 2.
    Agol VI, Paul AV, Wimmer E (1999) Paradoxes of the replication of picornaviral genomes. Virus Res 62:129–147CrossRefGoogle Scholar
  3. 3.
    Alexanderson S, Knowles NJ, Dekker A, Belsham GJ, Zhang Z, Koenen F (2012) In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW (eds), Disease of swine, 10th edn. Blackwell Publishing, Inc., Oxford, pp 587–620Google Scholar
  4. 4.
    Arruda PH, Arruda BL, Schwartz KJ, Vannucci F, Resende T, Rovira A, Sundberg P, Nietfeld J, Hause BM (2017) Detection of a novel sapelovirus in central nervous tissue of pigs with polioencephalomyelitis in the USA. Transbound Emerg Dis 64:311–315CrossRefGoogle Scholar
  5. 5.
    Auerbach J, Prager D, Neuhaus S, Loss U, Witte KH (1994) Grouping of porcine enteroviruses by indirect immunofluorescence and description of two new serotypes. Zent Vet B 41:277–282Google Scholar
  6. 6.
    Bai H, Liu J, Fang L, Kataoka M, Takeda N, Wakita T, Li TC (2018) Characterization of porcine sapelovirus isolated from Japanese swine with PLC/PRF/5 cells. Transbound Emerg Dis 65:727–734CrossRefGoogle Scholar
  7. 7.
    Belsham GJ (2009) Divergent picornavirus IRES elements. Virus Res 139:183–192CrossRefGoogle Scholar
  8. 8.
    Brown DM, Cornell CT, Tran GP, Nguyen JH, Semler BL (2005) An authentic 3′-noncoding region is necessary for efficient poliovirus replication. J Virol 79:11962–11973CrossRefGoogle Scholar
  9. 9.
    Buitrago D, Cano-Gómez C, Agüero M, Fernandez-Pacheco P, Gómez-Tejedor C, Jiménez-Clavero MA (2010) A survey of porcine picornaviruses and adenoviruses in fecal samples in Spain. J Vet Diagn Investig 22:763–766CrossRefGoogle Scholar
  10. 10.
    Cano-Gómez C, García-Casado MA, Soriguer R, Palero F, Jiménez-Clavero MA (2013) Teschoviruses and sapeloviruses in faecal samples from wild boar in Spain. Vet Microbiol 165:115–122CrossRefGoogle Scholar
  11. 11.
    Cordey S, Gerlach D, Junier T, Zdobnov EM, Kaiser L, Tapparel C (2008) The cis-acting replication elements define human enterovirus and rhinovirus species. RNA 14:1568–1578CrossRefGoogle Scholar
  12. 12.
    Chard LS, Kaku Y, Jones B, Nayak A, Belsham GJ (2006) Functional analyses of RNA structures shared between the internal ribosome entry sites of hepatitis C virus and the picornavirus porcine teschovirus 1 Talfan. J Virol 80:1271–1279CrossRefGoogle Scholar
  13. 13.
    Chen J, Chen F, Zhou Q, Li W, Song Y, Pan Y, Zhang X, Xue C, Bi Y, Cao Y (2012) Complete genome sequence of a novel porcine Sapelovirus strain YC2011 isolated from piglets with diarrhea. J Virol 86:10898CrossRefGoogle Scholar
  14. 14.
    Chen Q, Zheng Y, Guo B, Zhang J, Yoon KJ, Harmon KM, Main RG, Li G (2016) Complete genome sequence of porcine sapelovirus strain USA/IA33375/2015 identified in the United States. Genome Announc 4:e01055–e01016Google Scholar
  15. 15.
    Chen Q, Wang L, Zheng Y, Zhang J, Guo B, Yoon KJ, Gauger PC, Harmon KM, Main RG, Li G (2018) Metagenomic analysis of the RNA fraction of the fecal virome indicates high diversity in pigs infected by porcine endemic diarrhea virus in the United States. Virol J 15:95CrossRefGoogle Scholar
  16. 16.
    Donin DG, de Arruda Leme R, Alfieri AF, Alberton GC, Alfieri AA (2014) First report of Porcine teschovirus (PTV), Porcine sapelovirus (PSV) and Enterovirus G (EV-G) in pig herds of Brazil. Trop Anim Health Prod 46:523–528CrossRefGoogle Scholar
  17. 17.
    Dunne HW, Gobble JL, Hokanson JF, Kradel DC, Bubash GR (1965) Porcine reproductive failure associated with a newly identified “SMEDI” group of picorna viruses. Am J Vet Res 26:1284–1297Google Scholar
  18. 18.
    Dunne HW, Wang JT, Ammerman EH (1971) Classification of North American porcine enteroviruses: a comparison with European and Japanese strains. Infect Immun 4:619–631Google Scholar
  19. 19.
    Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  20. 20.
    Fernández-Miragall O, López de Quinto S, Martínez-Salas E (2009) Relevance of RNA structure for the activity of picornavirus IRES elements. Virus Res 139:172–182CrossRefGoogle Scholar
  21. 21.
    Honda E, Hattori I, Oohara Y, Taniguchi T, Ariyama K, Kimata A, Nagamine N, Kumagai T (1990) Sero- and CPE-types of porcine enteroviruses isolated from healthy and diarrheal pigs: possible association of CPE type II with diarrhea. Nihon Juigaku Zasshi 52:85–90CrossRefGoogle Scholar
  22. 22.
    Huang J, Gentry RF, Zarkower A (1980) Experimental infection of pregnant sows with porcine enteroviruses. Am J Vet Res 41:469–473Google Scholar
  23. 23.
    Jacobson SJ, Konings DA, Sarnow P (1993) Biochemical and genetic evidence for a pseudoknot structure at the 3′-terminus of the poliovirus RNA genome and its role in viral RNA amplification. J Virol 67:2961–2971Google Scholar
  24. 24.
    Kaku Y, Sarai A, Murakami Y (2001) Genetic reclassification of porcine enteroviruses. J Gen Virol 82:417–424CrossRefGoogle Scholar
  25. 25.
    Kim DS, Kang MI, Son KY, Bak GY, Park JG, Hosmillo M, Seo JY, Kim JY, Alfajaro MM, Soliman M, Baek YB, Cho EH, Lee JH, Kwon J, Choi JS, Goodfellow I, Cho KO (2016) Pathogenesis of Korean Sapelovirus A in piglets and chicks. J Gen Virol 97:2566–2574CrossRefGoogle Scholar
  26. 26.
    Knowles NJ, Buckley LS, Pereira HG (1979) Classification of porcine enteroviruses by antigenic analysis and cytopathic effects in tissue culture: description of 3 new serotypes. Arch Virol 62:201–208CrossRefGoogle Scholar
  27. 27.
    Krumbholz A, Dauber M, Henke A, Birch-Hirschfeld E, Knowles NJ, Stelzner A, Zell R (2002) Sequencing of porcine enterovirus groups II and III reveals unique features of both virus groups. J Virol 76:5813–5821CrossRefGoogle Scholar
  28. 28.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  29. 29.
    Lan D, Ji W, Yang S, Cui L, Yang Z, Yuan C, Hua X (2011) Isolation and characterization of the first Chinese porcine sapelovirus strain. Arch Virol 156:1567–1574CrossRefGoogle Scholar
  30. 30.
    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 73:152–160Google Scholar
  31. 31.
    Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463CrossRefGoogle Scholar
  32. 32.
    Melchers WJ, Hoenderop JG, Bruins Slot HJ, Pleij CW, Pilipenko EV, Agol VI, Galama JM (1997) Kissing of the two predominant hairpin loops in the coxsackie B virus 3′-untranslated region is the essential structural feature of the origin of replication required for negative-strand RNA synthesis. J Virol 71:686–696Google Scholar
  33. 33.
    Nagai M, Omatsu T, Aoki H, Otomaru K, Uto T, Koizumi M, Minami-Fukuda F, Takai H, Murakami T, Masuda T, Yamasato H, Shiokawa M, Tsuchiaka S, Naoi Y, Sano K, Okazaki S, Katayama Y, Oba M, Furuya T, Shirai J, Mizutani T (2015) Full genome analysis of bovine astrovirus from fecal samples of cattle in Japan: identification of possible interspecies transmission of bovine astrovirus. Arch Virol 160:2491–2501CrossRefGoogle Scholar
  34. 34.
    Oberste MS, Maher K, Kilpatrick DR, Pallansch MA (1999) Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948Google Scholar
  35. 35.
    Paul AV, Yin J, Mugavero J, Rieder E, Liu Y, Wimmer E (2003) A “slide-back” mechanism for the initiation of protein-primed RNA synthesis by the RNA polymerase of poliovirus. J Biol Chem 278:43951–43960CrossRefGoogle Scholar
  36. 36.
    Pilipenko EV, Poperechny KV, Maslova SV, Melchers WJ, Slot HJ, Agol VI (1996) Cis-element, oriR, involved in the initiation of (−) strand poliovirus RNA: a quasi-globular multi-domain RNA structure maintained by tertiary (“kissing”) interactions. EMBO J 15:5428–5436CrossRefGoogle Scholar
  37. 37.
    Pisarev AV, Chard LS, Kaku Y, Johns HL, Shatsky IN, Belsham GJ (2003) Functional and structural similarities between the internal ribosome entry sites of hepatitis C virus and porcine teschovirus, a picornavirus. J Virol 78:4487–4497CrossRefGoogle Scholar
  38. 38.
    Prodělalová J (2012) The survey of porcine teschoviruses, sapeloviruses and enteroviruses B infecting domestic pigs and wild boars in the Czech Republic between 2005 and 2011. Infect Genet Evol 12:1447–1451CrossRefGoogle Scholar
  39. 39.
    Ray PK, Desingu PA, Kumari S, John JK, Sethi M, Sharma GK, Pattnaik B, Singh RK, Saikumar G (2018) Porcine sapelovirus among diarrhoeic piglets in India. Transbound Emerg Dis 65:261–263CrossRefGoogle Scholar
  40. 40.
    Rieder E, Paul AV, Kim DW, van Boom JH, Wimmer E (2000) Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation. J Virol 74:10371–10380CrossRefGoogle Scholar
  41. 41.
    Schock A, Gurrala R, Fuller H, Foyle L, Dauber M, Martelli F, Scholes S, Roberts L, Steinbach F, Dastjerdi A (2014) Investigation into an outbreak of encephalomyelitis caused by a neuroinvasive porcine sapelovirus in the United Kingdom. Vet Microbiol 172:381–389CrossRefGoogle Scholar
  42. 42.
    Son KY, Kim DS, Kwon J, Choi JS, Kang MI, Belsham GJ, Cho KO (2014) Full-length genomic analysis of Korean porcine Sapelovirus strains. PLoS ONE 9:e107860CrossRefGoogle Scholar
  43. 43.
    Son KY, Kim DS, Matthijnssens J, Kwon HJ, Park JG, Hosmillo M, Alfajaro MM, Ryu EH, Kim JY, Kang MI, Cho KO (2014) Molecular epidemiology of Korean porcine sapeloviruses. Arch Virol 159:1175–1180CrossRefGoogle Scholar
  44. 44.
    Sozzi E, Barbieri I, Lavazza A, Lelli D, Moreno A, Canelli E, Bugnetti M, Cordioli P (2010) Molecular characterization and phylogenetic analysis of VP1 of porcine enteric picornaviruses isolates in Italy. Transbound Emerg Dis 57:434–442CrossRefGoogle Scholar
  45. 45.
    Sweeney TR, Dhote V, Yu Y, Hellen CU (2011) A distinct class of internal ribosomal entry site in members of the Kobuvirus and proposed Salivirus and Paraturdivirus genera of the Picornaviridae. J Virol 86:1468–1486CrossRefGoogle Scholar
  46. 46.
    Tapparel C, Siegrist F, Petty TJ, Kaiser L (2013) Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 14:282–293CrossRefGoogle Scholar
  47. 47.
    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 25:4876–4882CrossRefGoogle Scholar
  48. 48.
    Tsuchiaka S, Naoi Y, Imai R, Masuda T, Ito M, Akagami M, Ouchi Y, Ishii K, Sakaguchi S, Omatsu T, Katayama Y, Oba M, Shirai J, Satani Y, Takashima Y, Taniguchi Y, Takasu M, Madarame H, Sunaga F, Aoki H, Makino S, Mizutani T, Nagai M (2018) Genetic diversity and recombination of enterovirus G strains in Japanese pigs: high prevalence of strains carrying a papain-like cysteine protease sequence in the enterovirus G population. PLoS ONE 11(1):e0190819 13(CrossRefGoogle Scholar
  49. 49.
    Van Dung N, Anh PH, Van Cuong N, Hoa NT, Carrique-Mas J, Hien VB, Campbell J, Baker S, Farrar J, Woolhouse ME, Bryant JE, Simmonds P (2014) Prevalence, genetic diversity and recombination of species G enteroviruses infecting pigs in Vietnam. J Gen Virol 95:549–556CrossRefGoogle Scholar
  50. 50.
    Van Dung N, Anh PH, Van Cuong N, Hoa NT, Carrique-Mas J, Hien VB, Sharp C, Rabaa M, Berto A, Campbell J, Baker S, Farrar J, Woolhouse ME, Bryant JE, Simmonds P (2016) Large-scale screening and characterization of enteroviruses and kobuviruses infecting pigs in Vietnam. J Gen Virol 97:378–388CrossRefGoogle Scholar
  51. 51.
    Yang T, Li R, Peng W, Ge M, Luo B, Qu T, Yu X (2017) First isolation and genetic characteristics of porcine sapeloviruses in Hunan, China. Arch Virol 162:1589–1597CrossRefGoogle Scholar
  52. 52.
    Yang T, Yu X, Yan M, Luo B, Li R, Qu T, Luo Z, Ge M, Zhao D (2017) Molecular characterization of Porcine sapelovirus in Hunan, China. J Gen Virol 98:2738–2747CrossRefGoogle Scholar
  53. 53.
    Yu Y, Sweeney TR, Kafasla P, Jackson RJ, Pestova TV, Hellen CU (2011) The mechanism of translation initiation on Aichivirus RNA mediated by a novel type of picornavirus IRES. EMBO J 30:4423–4436CrossRefGoogle Scholar
  54. 54.
    Zell R, Dauber M, Krumbholz A, Henke A, Birch-Hirschfeld E, Stelzner A, Prager D, Wurm R (2001) Porcine teschoviruses comprise at least eleven distinct serotypes: molecular and evolutionary aspects. J Virol 75:1620–1631CrossRefGoogle Scholar
  55. 55.
    Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, Simmonds P, Skern T, Stanway G, Yamashita T, ICTV Report Consortium (2017) ICTV virus taxonomy profile: Picornaviridae. J Gen Virol 98:2421–2422CrossRefGoogle Scholar
  56. 56.
    Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Fujiko Sunaga
    • 1
  • Tsuneyuki Masuda
    • 2
  • Mika Ito
    • 3
  • Masataka Akagami
    • 4
  • Yuki Naoi
    • 5
  • Kaori Sano
    • 5
  • Yukie Katayama
    • 5
  • Tsutomu Omatsu
    • 5
  • Mami Oba
    • 5
  • Shoichi Sakaguchi
    • 5
    • 6
  • Tetsuya Furuya
    • 7
  • Hiroshi Yamasato
    • 2
  • Yoshinao Ouchi
    • 4
  • Junsuke Shirai
    • 5
    • 7
  • Tetsuya Mizutani
    • 5
  • Makoto Nagai
    • 1
    • 5
    Email author
  1. 1.School of Veterinary MedicineAzabu UniversitySagamiharaJapan
  2. 2.Kurayoshi Livestock Hygiene Service CenterKurayoshiJapan
  3. 3.Ishikawa Nanbu Livestock Hygiene Service CenterKanazawaJapan
  4. 4.Kenpoku Livestock Hygiene Service CenterMitoJapan
  5. 5.Research and Education Center for Prevention of Global Infectious Disease of AnimalsTokyo University of Agriculture and TechnologyFuchuJapan
  6. 6.Department of Microbiology and Infection ControlOsaka Medical CollegeOsakaJapan
  7. 7.Cooperative Department of Veterinary Medicine, Faculty of AgricultureTokyo University of Agriculture and TechnologyFuchuJapan

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