Abstract
Porcine sapelovirus (PSV) infections have been associated with a wide spectrum of symptoms, ranging from asymptomatic infection to clinical signs including diarrhoea, pneumonia, reproductive disorders, and polioencephalomyelitis. Although it has a global distribution, there have been relatively few studies on PSV in domestic animals. We isolated a PSV strain, SHCM2019, from faecal specimens from swine, using PK-15 cells. To investigate its molecular characteristics and pathogenicity, the genomic sequence of strain SHCM2019 was analysed, and clinical manifestations and pathological changes occurring after inoculation of neonatal piglets were observed. The virus isolated using PK-15 cells was identified as PSV using RT-PCR, transmission electron microscopy (TEM), and immunofluorescence assay (IFA). Sequencing results showed that the full-length genome of the SHCM2019 strain was 7,567 nucleotides (nt) in length, including a 27-nucleotide poly(A) tail. Phylogenetic analysis demonstrated that this virus was a PSV isolate belonging to the Chinese strain cluster. Recombination analysis indicated that there might be a recombination breakpoint upstream of the 3D region of the genome. Pathogenicity experiments demonstrated that the virus isolate could cause diarrhoea and pneumonia in piglets. In breif, a recombinant PSV strain, SHCM2019, was isolated and shown to be pathogenic. Our results may provide a reference for future research on the pathogenic mechanism and evolutionary characteristics of PSV.
Similar content being viewed by others
Availability of data and materials
Data supporting the conclusions of this article are presented in the manuscript.
Abbreviations
- PSV:
-
Porcine sapelovirus
- PEV-8:
-
Porcine enterovirus 8
- UTR:
-
Untranslated region
- ORF:
-
Open reading frame
- DMEM:
-
Dulbecco′s modified Eagle′s medium
- FBS:
-
Foetal bovine serum
- PKV:
-
Porcine kobuvirus
- PAstV:
-
Porcine astrovirus
- PDCoV:
-
Porcine deltacoronavirus
- PToV:
-
Porcine torovirus
- PTV:
-
Porcine teschovirus
- PSaV:
-
Porcine sapovirus
- PEDV:
-
Porcine epidemic diarrhoea virus
- TGEV:
-
Transmissible gastroenteritis virus
- PoRV:
-
Porcine rotavirus
- BVDV:
-
Bovine viral diarrhoea virus
- PCV2:
-
Porcine circovirus type 2
- CPE:
-
Cytopathic effect
- PBS:
-
Phosphate-buffered saline
- M-MLV:
-
Moloney murine leukaemia virus
- DEPC:
-
Diethylpyrocarbonate
- TEM:
-
Transmission electron microscopy
- IFA:
-
Immunofluorescence assay
- RT:
-
Room temperature
- BSA:
-
Bovine serum albumin
- DAPI:
-
Diamidino-phenylindole
- RDP:
-
Recombination detection program
- ELISA:
-
Enzyme-linked immunosorbent assay
References
Adams MJ, Lefkowitz EJ, King AM, Bamford DH, Breitbart M, Davison AJ, Ghabrial SA, Gorbalenya AE, Knowles NJ, Krell P, Lavigne R, Prangishvili D, Sanfacon H, Siddell SG, Simmonds P, Carstens EB (2015) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses. Arch Virol 160:1837–1850
Tseng CH, Tsai HJ (2007) Sequence analysis of a duck picornavirus isolate indicates that it together with porcine enterovirus type 8 and simian picornavirus type 2 should be assigned to a new picornavirus genus. Virus Res 129:104–114
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 76:5813–5821
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 86:10898
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:e107860
Lamont PH, Betts AO (1958) Enteroviruses in the pig. Nature 182:608–609
Buitrago D, Cano-Gomez C, Aguero M, Fernandez-Pacheco P, Gomez-Tejedor C, Jimenez-Clavero MA (2010) A survey of porcine picornaviruses and adenoviruses in fecal samples in Spain. J Vet Diagn Invest 22:763–766
L’Ecuyer C, Greig AS (1966) Serological and biological studies on porcine enteroviruses isolated in Canada. Can Vet J 7:148–154
Morimoto T, Watanabe M (1964) Serological Identification of Porcine Enteroviruses Isolated in Japan. Natl Inst Anim Health Q 4:177–182
Forman AJ, Pass DA, Connaughton ID (1982) The characterisation and pathogenicity of porcine enteroviruses isolated in Victoria. Aust Vet J 58:136–142
Donin DG, de Arruda LR, 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 46:523–528
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 156:1567–1574
Chelli E, De Sabato L, Vaccari G, Ostanello F, Di Bartolo I (2020) Detection and Characterization of Porcine Sapelovirus in Italian Pig Farms. Animals (Basel) 10(6):966
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 65:261–263
Boros A, Laszlo Z, Pankovics P, Marosi A, Albert M, Csagola A, Biro H, Fahsbender E, Delwart E, Reuter G (2020) High prevalence, genetic diversity and a potentially novel genotype of Sapelovirus A (Picornaviridae) in enteric and respiratory samples in Hungarian swine farms. J Gen Virol 101:609–621
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 12:1447–1451
Huang J, Gentry RF, Zarkower A (1980) Experimental infection of pregnant sows with porcine enteroviruses. Am J Vet Res 41:469–473
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 172:381–389
Zhang B, Tang C, Yue H, Ren Y, Song Z (2014) Viral metagenomics analysis demonstrates the diversity of viral flora in piglet diarrhoeic faeces in China. J Gen Virol 95:1603–1611
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 SapelovirusA in piglets and chicks. J Gen Virol 97:2566–2574
Shan T, Li L, Simmonds P, Wang C, Moeser A, Delwart E (2011) The fecal virome of pigs on a high-density farm. J Virol 85:11697–11708
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. J Virol 15:95–103
Domingo E, Sheldon J, Perales C (2012) Viral quasispecies evolution. Microbiol Mol Biol Rev 76:159–216
Sunaga F, Masuda T, Ito M, Akagami M, Naoi Y, Sano K, Katayama Y, Omatsu T, Oba M, Sakaguchi S, Furuya T, Yamasato H, Ouchi Y, Shirai J, Mizutani T, Nagai M (2019) Complete genomic analysis and molecular characterization of Japanese porcine sapeloviruses. Virus Genes 55:198–208
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 73:1941–1948
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 95:549–556
Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J (2003) Recombination in circulating enteroviruses. J Virol 77:10423–10431
Harima H, Kajihara M, Simulundu E, Bwalya E, Qiu Y, Isono M, Okuya K, Gonzalez G, Yamagishi J, Hang’ombe BM, Sawa H, Mweene AS, Takada A (2020) Genetic and Biological Diversity of Porcine Sapeloviruses Prevailing in Zambia. Viruses 12:180–193
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 98:2738–2747
Li B, Ma J, Liu Y, Wen L, Yu Z, Ni Y, Zhang X, Zhou J, Guo R, Wang X, Feng Z, Hu Y, Lv L, He K (2012) Complete genome sequence of a highly prevalent porcine circovirus 2 isolated from piglet stool samples in China. J Virol 86:4716
Sun RQ, Cai RJ, Chen YQ, Liang PS, Chen DK, Song CX (2012) Outbreak of porcine epidemic diarrhea in suckling piglets, China. Emerg Infect Dis 18:161–163
Funding
This research was funded by the 13th Five-Year National Key Research and Development Plan (No. 2018YFD0500102) and Shanghai Agriculture Applied Technology Development Program, China (Grant No. C20190302).
Author information
Authors and Affiliations
Contributions
HLL conceived and designed this study; NNL and BQL conducted experiments; JT, JHC, YS and XHS contributed their technical knowledge; NNL and HLL wrote this paper; BQL and TJ were involved in interpreting the results and critically reading the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict interest
All authors declare that they have no competing interests. Author details Institute of Animal Husbandry and Veterinary, Shanghai Academy of Agricultural Sciences, 2901 Beidi Road, Shanghai 201106, China.
Ethical approval
All animal experiments were performed under the guidance of the Institutional Animal Care and Use Committee at the Center for Disease Control and Prevention (CDC) and the Laboratory Animal Care International accredited facility.
Additional information
Handling Editor: Diego G. Diel
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.
Rights and permissions
About this article
Cite this article
Li, N., Tao, J., Li, B. et al. Molecular characterization of a porcine sapelovirus strain isolated in China. Arch Virol 166, 2683–2692 (2021). https://doi.org/10.1007/s00705-021-05153-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-021-05153-4