Molecular Detection and Characterization of Porcine Epidemic Diarrhea Virus and Porcine Aichivirus C Coinfection in México
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. RNA Extraction
2.3. Molecular Testing
2.4. Sequencing and Bioinformatics Analyses
2.5. Phylogenetic Analysis
2.6. Viral Culture
3. Results
3.1. Prevalence of Porcine Kobuvirus and Porcine Coronavirus in Diarrheic Pigs
3.2. Viral Genome Detection
3.3. Genome Analysis of Porcine Kobuvirus
3.4. Genome Analysis of the Porcine Epidemic Diarrhea Virus
3.5. Sequence Analysis of PSaV
3.6. Viral Culture
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sun, Y.G.; Li, R.; Xie, S.; Qiao, S.; Li, Q.; Chen, X.X.; Deng, R.; Zhang, G. Identification of a novel linear B-cell epitope within the collagenase equivalent domain of porcine epidemic diarrhea virus spike glycoprotein. Virus Res. 2019, 266, 34–42. [Google Scholar] [CrossRef]
- Zhang, F.; Luo, S.; Gu, J.; Li, Z.; Li, K.; Yuan, W.; Ye, Y.; Li, H.; Ding, Z.; Song, D.; et al. Prevalence and phylogenetic analysis of porcine diarrhea associated viruses in southern China from 2012 to 2018. BMC Vet. Res. 2019, 15, 470. [Google Scholar] [CrossRef] [Green Version]
- Stevenson, G.W.; Hoang, H.; Schwartz, K.J.; Burrough, E.R.; Sun, D.; Madson, D.; Cooper, V.L.; Pillatzki, A.; Gauger, P.; Schmitt, B.J.; et al. Emergence of Porcine epidemic diarrhea virus in the United States: Clinical signs, lesions, and viral genomic sequences. J. Vet. Diagn. Investig. 2013, 25, 649–654. [Google Scholar] [CrossRef] [Green Version]
- Trujillo-Ortega, M.E.; Beltrán-Figueroa, R.; García-Hernández, M.E.; Juárez-Ramírez, M.; Sotomayor-González, A.; Hernández-Villegas, E.N.; Becerra-Hernández, J.F.; Sarmiento-Silva, R.E. Isolation and characterization of porcine epidemic diarrhea virus associated with the 2014 disease outbreak in Mexico: Case report. BMC Vet. Res. 2016, 12, 132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hofmann, M.; Wyler, R. Quantitation, biological and physicochemical properties of cell culture-adapted porcine epidemic diarrhea coronavirus (PEDV). Vet. Microbiol. 1989, 20, 131–142. [Google Scholar] [CrossRef]
- Marthaler, D.; Jiang, Y.; Otterson, T.; Goyal, S.; Rossow, K.; Collins, J. Complete genome sequence of porcine epidemic diarrhea virus strain USA/Colorado/2013 from the United States. Genome Announc. 2013, 1, e00555-13. [Google Scholar] [CrossRef] [Green Version]
- Reuter, G.; Boldizsár, Á.; Kiss, I.; Pankovics, P. Candidate new species of Kobuvirus in porcine hosts. Emerg. Infect. Dis. 2008, 14, 1968. [Google Scholar] [CrossRef]
- Sisay, Z.; Wang, Q.; Oka, T.; Saif, L. Prevalence and molecular characterization of porcine enteric caliciviruses and first detection of porcine kobuviruses in US swine. Arch. Virol. 2013, 158, 1583–1588. [Google Scholar] [CrossRef] [Green Version]
- Yu, J.M.; Jin, M.; Zhang, Q.; Li, H.Y.; Li, D.D.; Xu, Z.Q.; Li, J.S.; Cui, S.X.; Yang, S.H.; Liu, N.; et al. Candidate porcine Kobuvirus, China. Emerg. Infect. Dis. 2009, 15, 823. [Google Scholar] [CrossRef] [PubMed]
- Barry, A.F.; Ribeiro, J.; Alfieri, A.F.; van der Poel, W.H.M.; Alfieri, A.A. First detection of kobuvirus in farm animals in Brazil and the Netherlands. Infect. Genet. Evol. 2011, 11, 1811–1814. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khamrin, P.; Maneekarn, N.; Kongkaew, A.; Kongkaew, S.; Okitsu, S.; Ushijima, H. Porcine kobuvirus in piglets, Thailand. Emerg. Infect. Dis. 2009, 15, 2075. [Google Scholar] [CrossRef]
- Khamrin, P.; Maneekarn, N.; Hidaka, S.; Kishikawa, S.; Ushijima, K.; Okitsu, S.; Ushijima, H. Molecular detection of kobuvirus sequences in stool samples collected from healthy pigs in Japan. Infect. Genet. Evol. 2010, 10, 950–954. [Google Scholar] [CrossRef]
- Park, S.J.; Kim, H.K.; Moon, H.J.; Song, D.S.; Rho, S.M.; Han, J.Y.; Nguyen, V.G.; Park, B.K. Molecular detection of porcine kobuviruses in pigs in Korea and their association with diarrhea. Arch. Virol. 2010, 155, 1803–1811. [Google Scholar] [CrossRef]
- Reuter, G.; Boldizsár, Á.; Pankovics, P. Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae. Arch. Virol. 2009, 154, 101. [Google Scholar] [CrossRef]
- Lefkowitz, E.J.; Dempsey, D.M.; Hendrickson, R.C.; Orton, R.J.; Siddell, S.G.; Smith, D.B. Virus taxonomy: The database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res. 2018, 46, D708–D717. [Google Scholar] [CrossRef] [Green Version]
- Jackova, A.; Sliz, I.; Mandelik, R.; Salamunova, S.; Novotny, J.; Kolesarova, M.; Vlasakova, M.; Vilcek, S. Porcine kobuvirus 1 in healthy and diarrheic pigs: Genetic detection and characterization of virus and co-infection with rotavirus A. Infect. Genet. Evol. 2017, 49, 73–77. [Google Scholar] [CrossRef]
- Zhou, W.; Ullman, K.; Chowdry, V.; Reining, M.; Benyeda, Z.; Baule, C.; Juremalm, M.; Wallgren, P.; Schwarz, L.; Zhou, E.; et al. Molecular investigations on the prevalence and viral load of enteric viruses in pigs from five European countries. Vet. Microbiol. 2016, 182, 75–81. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Z.P.; Yang, Z.; Lin, W.D.; Wang, W.Y.; Yang, J.; Jin, W.J.; Qin, A.J. The rate of co-infection for piglet diarrhea viruses in China and the genetic characterization of porcine epidemic diarrhea virus and porcine kobuvirus. Acta Virol. 2016, 60, 55–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, Z.; Ruan, H.; Qiao, S.; Deng, R.; Zhang, G. Co-infection status of porcine circoviruses (PCV2 and PCV3) and porcine epidemic diarrhea virus (PEDV) in pigs with watery diarrhea in Henan province, central China: Co-infection of PCV2, PCV3 and PEDV. Microb. Pathog. 2020, 142, 104047. [Google Scholar] [CrossRef] [PubMed]
- Jung, K.; Kang, B.K.; Lee, C.S.; Song, D.S. Impact of porcine group A rotavirus co-infection on porcine epidemic diarrhea virus pathogenicity in piglets. Res. Vet. Sci. 2008, 84, 502–506. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Wang, L.; Zheng, Y.; Zhang, J.; Guo, B.; Yoon, K.J.; Gauger, P.C.; Harmon, K.M.; Main, R.G.; Li, G. 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. 2018, 15, 95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, W.; Godzik, A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22, 1658–1659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, M.; Li, C.; Qi, S.; Yang, D.; Jiang, N.; Yin, B.; Guo, D.; Kong, F.; Yuan, D.; Feng, L.; et al. A molecular epidemiological investigation of PEDV in China: Characterization of co-infection and genetic diversity of S1-based genes. Transbound. Emerg. Dis. 2020, 67, 1129–1140. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Bartolo, I.; Tofani, S.; Angeloni, G.; Ponterio, E.; Ostanello, F.; Ruggeri, F.M. Detection and characterization of porcine caliciviruses in Italy. Arch. Virol. 2014, 159, 2479–2484. [Google Scholar] [CrossRef]
- Bushnell, B. BBMap: A Fast, Accurate, Splice-Aware Aligner; Lawrence Berkeley National Lab.(LBNL): Berkeley, CA, USA, 2014. [Google Scholar]
- Martin, D.P.; Murrell, B.; Golden, M.; Khoosal, A.; Muhire, B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015, 1, vev003. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.-L.; Zhu, L.; Ma, J.-Y.; Zhou, Q.-F.; Song, Y.-H.; Sun, B.-L.; Chen, R.-A.; Xie, Q.-M.; Bee, Y.-Z. Molecular characterization and phylogenetic analysis of porcine epidemic diarrhea virus (PEDV) field strains in south China. Virus Genes 2012, 45, 181–185. [Google Scholar] [CrossRef]
- Liu, P.; Du, R.J.; Wang, L.; Han, J.; Liu, L.; Zhang, Y.L.; Xia, J.K.; Lu, F.M.; Zhuang, H. Management of Hepatitis E Virus (HEV) zoonotic transmission: Protection of rabbits against HEV challenge following immunization with HEV 239 vaccine. PLoS ONE 2014, 9, e87600. [Google Scholar] [CrossRef]
- Hu, H.; Jung, K.; Vlasova, A.N.; Chepngeno, J.; Lu, Z.; Wang, Q.; Saif, L.J. Isolation and characterization of porcine deltacoronavirus from pigs with diarrhea in the United States. J. Clin. Microbiol. 2015, 53, 1537–1548. [Google Scholar] [CrossRef] [Green Version]
- Andrews, S. FASTQC A Quality Control tool for High Throughput Sequence Data. 2015. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (accessed on 13 April 2021).
- Wang, Q.H.; Souza, M.; Funk, J.A.; Zhang, W.; Saif, L.J. Prevalence of noroviruses and sapoviruses in swine of various ages determined by reverse transcription-PCR and microwell hybridization assays. J. Clin. Microbiol. 2006, 44, 2057–2062. [Google Scholar] [CrossRef] [Green Version]
- Nurk, S.; Bankevich, A.; Antipov, D.; Gurevich, A.A.; Korobeynikov, A.; Lapidus, A.; Prjibelski, A.D.; Pyshkin, A.; Sirotkin, A.; Sirotkin, Y.; et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J. Comput. Biol. 2013, 20, 714–737. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boetzer, M.; Henkel, C.V.; Jansen, H.J.; Butler, D.; Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011, 27, 578–579. [Google Scholar] [CrossRef] [Green Version]
- Nurk, S.; Bankevich, A.; Antipov, D.; Gurevich, A.; Korobeynikov, A.; Lapidus, A.; Prjibelsky, A.; Pyshkin, A.; Sirotkin, A.; Sirotkin, Y.; et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Research in Computational Molecular Biology; Lecture Notes in Computer Science; Springer: Berlin/Heidelberg, Germany, 2013. [Google Scholar]
- Wood, D.E.; Salzberg, S.L. Kraken: Ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014, 15, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guindon, S.; Lethiec, F.; Duroux, P.; Gascuel, O. PHYML Online—A web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 2005, 33 (Suppl. 2), W557–W559. [Google Scholar] [CrossRef] [Green Version]
- Letunic, I.; Bork, P. Interactive Tree Of Life (iTOL): An online tool for phylogenetic tree display and annotation. Bioinformatics 2007, 23, 127–128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. JModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [PubMed] [Green Version]
- Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [Green Version]
- Lara-Romero, R.; Gómez-Núñez, L.; Cerriteño-Sánchez, J.L.; Márquez-Valdelamar, L.; Mendoza-Elvira, S.; Ramírez-Mendoza, H.; Rivera-Benítez, J.F. Molecular characterization of the spike gene of the porcine epidemic diarrhea virus in Mexico, 2013–2016. Virus Genes 2018, 54, 215–224. [Google Scholar] [CrossRef]
- Chen, Q.; Gauger, P.C.; Stafne, M.R.; Thomas, J.T.; Madson, D.M.; Huang, H.; Zheng, Y.; Li, G.; Zhang, J. Pathogenesis comparison between the United States porcine epidemic diarrhoea virus prototype and S-INDEL-variant strains in conventional neonatal piglets. J. Gen. Virol. 2016, 97, 1107–1121. [Google Scholar] [CrossRef] [Green Version]
- Pérez-Rivera, C.; Ramírez-Mendoza, H.; Mendoza-Elvira, S.; Segura-Velázquez, R.; Sánchez-Betancourt, J.I. First report and phylogenetic analysis of porcine deltacoronavirus in Mexico. Transbound. Emerg. Dis. 2019, 66, 1436–1441. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Lan, X.; Yang, B. Molecular Epidemiological Investigation of Porcine kobuvirus and Its Coinfection Rate with PEDV and SaV in Northwest China. BioMed Res. Int. 2016, 2016, 1–6. [Google Scholar] [CrossRef] [PubMed]
Sample ID | Number of Filtered Reads | Assembled Contigs | Viral Swine Families | No. of Matched Reads | Scaffold Length (nt) | Mean Coverage |
---|---|---|---|---|---|---|
205H | 8,606,544.00 | 360 | Coronaviridae | 309,090 | 28,029 | 827.06 |
Picornaviridae | 186,517 | 8116 | 1723.60 | |||
Caliciviridae | 402 | 2977 | 10.13 | |||
103H | 5,451,484.00 | 333 | Coronavidae | 119,986 | 28,034 | 321.00 |
Picornaviridae | 336 | 580 | 43.45 |
Sample ID | Assembled Genome (AC Number) | Length (nt) | Subject Cover | Best Hit (BLASTn) (AC Number) | Perc. Identity (AC Number) |
---|---|---|---|---|---|
205H | EdoMex/205/2018 (MT490316.1) | 28,029 | 99.97% | Porcine epidemic diarrhea virus strain USA/Colorado/2013 (KF272920.1) | 99.66% (95.89%) |
EdoMex/2018/205 (MT211964.1) | 8116 | 99.50% | Porcine kobuvirus isolate OH/RV11/2011 (MF506730.1) | 90.66% (97.84%) | |
EdoMex/2018/205 (MT726205.1) | 2977 | 40.30% | Sapovirus GIII isolate p2 (KX688107.1) | 91.13% (96.64%) | |
103H | EdoMex/103/2018 (MT490315.1) | 28,034 | 99.99% | Porcine epidemic diarrhea virus strain USA/Colorado/2013 (KF272920.1) | 99.66% (95.89%) |
NA | 580 | 10% | Porcine kobuvirus strain KobuV/Pig-wt/ESP/P2B/2017 (MK962329.1) | 95.86% (100%) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
García-Hernández, M.-E.; Trujillo-Ortega, M.-E.; Alcaraz-Estrada, S.-L.; Lozano-Aguirre-Beltrán, L.; Sandoval-Jaime, C.; Taboada-Ramírez, B.I.; Sarmiento-Silva, R.-E. Molecular Detection and Characterization of Porcine Epidemic Diarrhea Virus and Porcine Aichivirus C Coinfection in México. Viruses 2021, 13, 738. https://doi.org/10.3390/v13050738
García-Hernández M-E, Trujillo-Ortega M-E, Alcaraz-Estrada S-L, Lozano-Aguirre-Beltrán L, Sandoval-Jaime C, Taboada-Ramírez BI, Sarmiento-Silva R-E. Molecular Detection and Characterization of Porcine Epidemic Diarrhea Virus and Porcine Aichivirus C Coinfection in México. Viruses. 2021; 13(5):738. https://doi.org/10.3390/v13050738
Chicago/Turabian StyleGarcía-Hernández, Montserrat-Elemi, María-Elena Trujillo-Ortega, Sofía-Lizbeth Alcaraz-Estrada, Luis Lozano-Aguirre-Beltrán, Carlos Sandoval-Jaime, Blanca Itzel Taboada-Ramírez, and Rosa-Elena Sarmiento-Silva. 2021. "Molecular Detection and Characterization of Porcine Epidemic Diarrhea Virus and Porcine Aichivirus C Coinfection in México" Viruses 13, no. 5: 738. https://doi.org/10.3390/v13050738
APA StyleGarcía-Hernández, M.-E., Trujillo-Ortega, M.-E., Alcaraz-Estrada, S.-L., Lozano-Aguirre-Beltrán, L., Sandoval-Jaime, C., Taboada-Ramírez, B. I., & Sarmiento-Silva, R.-E. (2021). Molecular Detection and Characterization of Porcine Epidemic Diarrhea Virus and Porcine Aichivirus C Coinfection in México. Viruses, 13(5), 738. https://doi.org/10.3390/v13050738