1887

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Volume 96, Issue 7

Global molecular genetic analysis of porcine circovirus type 2 (PCV2) sequences confirms the presence of four main PCV2 genotypes and reveals a rapid increase of PCV2d Free

Abstract

The oldest porcine circovirus type 2 (PCV2) sequence dates back to 1962 and is among several hundreds of publicly available PCV2 sequences. Despite this resource, few studies have investigated the global genetic diversity of PCV2. To evaluate the phylogenetic relationship of PCV2 strains, 1680 PCV2 open reading frame 2 (ORF2) sequences were compared and analysed by methods of neighbour-joining, maximum-likelihood, Bayesian inference and network analysis. Four distinct clades were consistently identified and included PCV2a, PCV2b, PCV2c and PCV2d; the -distance between PCV2d and PCV2b was 0.055±0.008, larger than the PCV2 genotype-definition cut-off of 0.035, supporting PCV2d as an independent genotype. Among the 1680 sequences, 278–285 (16.5–17 %) were classified as PCV2a, 1007–1058 (59.9–63 %) as PCV2b, three (0.2 %) as PCV2c and 322–323 (19.2 %) as PCV2d, with the remaining 12–78 sequences (0.7–4.6 %) classified as intermediate clades or strains by the various methods. Classification of strains to genotypes differed based on the number of sequences used for the analysis, indicating that sample size is important when determining classification and assessing PCV2 trends and shifts. PCV2d was initially identified in 1999 in samples collected in Switzerland, now appears to be widespread in China and has been present in North America since 2012. During 2012–2013, 37 % of all investigated PCV2 sequences from US pigs were classified as PCV2d and overall data analysis suggests an ongoing genotype shift from PCV2b towards PCV2d. The present analyses indicate that PCV2d emerged approximately 20 years ago.

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© 2015 The Authors
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2015-07-01
2024-04-23
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References

  1. Bandelt H. J., Forster P., Röhl A. (1999). Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16, 37–48. [View Article][PubMed] [Google Scholar]
  2. Bapteste E., van Iersel L., Janke A., Kelchner S., Kelk S., McInerney J. O., Morrison D. A., Nakhleh L., Steel M. et al. (2013). Networks: expanding evolutionary thinking. Trends Genet 29, 439–441. [View Article][PubMed] [Google Scholar]
  3. Beach N. M., Meng X. J. (2012). Efficacy and future prospects of commercially available and experimental vaccines against porcine circovirus type 2 (PCV2). Virus Res 164, 33–42. [View Article][PubMed] [Google Scholar]
  4. Cai L., Ni J., Xia Y., Zi Z., Ning K., Qiu P., Li X., Wang B., Liu Q. et al. (2012). Identification of an emerging recombinant cluster in porcine circovirus type 2. Virus Res 165, 95–102. [View Article][PubMed] [Google Scholar]
  5. Cheung A. K. (2003). Transcriptional analysis of porcine circovirus type 2. Virology 305, 168–180. [View Article][PubMed] [Google Scholar]
  6. Cheung A. K. (2009). Homologous recombination within the capsid gene of porcine circovirus type 2 subgroup viruses via natural co-infection. Arch Virol 154, 531–534. [View Article][PubMed] [Google Scholar]
  7. Cheung A. K., Lager K. M., Kohutyuk O. I., Vincent A. L., Henry S. C., Baker R. B., Rowland R. R., Dunham A. G. (2007). Detection of two porcine circovirus type 2 genotypic groups in United States swine herds. Arch Virol 152, 1035–1044. [View Article][PubMed] [Google Scholar]
  8. Cortey M., Olvera A., Grau-Roma L., Segalés J. (2011). Further comments on porcine circovirus type 2 (PCV2) genotype definition and nomenclature. Vet Microbiol 149, 522–523. [View Article][PubMed] [Google Scholar]
  9. Drummond A. J., Suchard M. A., Xie D., Rambaut A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29, 1969–1973. [View Article][PubMed] [Google Scholar]
  10. Duffy S., Shackelton L. A., Holmes E. C. (2008). Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9, 267–276. [View Article][PubMed] [Google Scholar]
  11. Dupont K., Nielsen E. O., Baekbo P., Larsen L. E. (2008). Genomic analysis of PCV2 isolates from Danish archives and a current PMWS case-control study supports a shift in genotypes with time. Vet Microbiol 128, 56–64. [View Article][PubMed] [Google Scholar]
  12. Elena S. F., Miralles R., Cuevas J. M., Turner P. E., Moya A. (2000). The two faces of mutation: extinction and adaptation in RNA viruses. IUBMB Life 49, 5–9. [View Article][PubMed] [Google Scholar]
  13. Firth C., Charleston M. A., Duffy S., Shapiro B., Holmes E. C. (2009). Insights into the evolutionary history of an emerging livestock pathogen: porcine circovirus 2. J Virol 83, 12813–12821. [View Article][PubMed] [Google Scholar]
  14. Guo L. J., Lu Y. H., Wei Y. W., Huang L. P., Liu C. M. (2010). Porcine circovirus type 2 (PCV2): genetic variation and newly emerging genotypes in China. Virol J 7, 273. [View Article][PubMed] [Google Scholar]
  15. Guo L., Fu Y., Wang Y., Lu Y., Wei Y., Tang Q., Fan P., Liu J., Zhang L. et al. (2012). A porcine circovirus type 2 (PCV2) mutant with 234 amino acids in capsid protein showed more virulence in vivo, compared with classical PCV2a/b strain. PLoS ONE 7, e41463. [View Article][PubMed] [Google Scholar]
  16. Hall T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41, 95–98. [Google Scholar]
  17. Hamel A. L., Lin L. L., Nayar G. P. (1998). Nucleotide sequence of porcine circovirus associated with postweaning multisystemic wasting syndrome in pigs. J Virol 72, 5262–5267.[PubMed] [Google Scholar]
  18. He J., Cao J., Zhou N., Jin Y., Wu J., Zhou J. (2013). Identification and functional analysis of the novel ORF4 protein encoded by porcine circovirus type 2. J Virol 87, 1420–1429. [View Article][PubMed] [Google Scholar]
  19. Huelsenbeck J. P., Ronquist F., Nielsen R., Bollback J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314. [View Article][PubMed] [Google Scholar]
  20. Huynh T. M., Nguyen B. H., Nguyen V. G., Dang H. A., Mai T. N., Tran T. H., Ngo M. H., Le V. T., Vu T. N. et al. (2014). Phylogenetic and phylogeographic analyses of porcine circovirus type 2 among pig farms in Vietnam. Transbound Emerg Dis 61, e25–e34. [CrossRef] [Google Scholar]
  21. Jacobsen B., Krueger L., Seeliger F., Bruegmann M., Segalés J., Baumgaertner W. (2009). Retrospective study on the occurrence of porcine circovirus 2 infection and associated entities in Northern Germany. Vet Microbiol 138, 27–33. [View Article][PubMed] [Google Scholar]
  22. Kim H. H., Park S. I., Hyun B. H., Park S. J., Jeong Y. J., Shin D. J., Chun Y. H., Hosmillo M., Lee B. J. et al. (2009). Genetic diversity of porcine circovirus type 2 in Korean pigs with postweaning multisystemic wasting syndrome during 2005–2007. J Vet Med Sci 71, 349–353. [CrossRef] [Google Scholar]
  23. Knell S., Willems H., Hertrampf B., Reiner G. (2005). Comparative genetic characterization of porcine circovirus type 2 samples from German wild boar populations. Vet Microbiol 109, 169–177. [CrossRef] [Google Scholar]
  24. Lefebvre D. J., Costers S., Van Doorsselaere J., Misinzo G., Delputte P. L., Nauwynck H. J. (2008). Antigenic differences among porcine circovirus type 2 strains, as demonstrated by the use of monoclonal antibodies. J Gen Virol 89, 177–187. [CrossRef] [Google Scholar]
  25. Librado P., Rozas J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452. [View Article][PubMed] [Google Scholar]
  26. Liu J., Chen I., Kwang J. (2005). Characterization of a previously unidentified viral protein in porcine circovirus type 2-infected cells and its role in virus-induced apoptosis. J Virol 79, 8262–8274. [View Article][PubMed] [Google Scholar]
  27. Mankertz A., Mankertz J., Wolf K., Buhk H. J. (1998). Identification of a protein essential for replication of porcine circovirus. J Gen Virol 79, 381–384.[PubMed] [Google Scholar]
  28. Martin D. P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26, 2462–2463. [View Article][PubMed] [Google Scholar]
  29. Martin D. P., Lemey P., Posada D. (2011). Analysing recombination in nucleotide sequences. Mol Ecol Resour 11, 943–955. [View Article][PubMed] [Google Scholar]
  30. Meehan B. M., McNeilly F., Todd D., Kennedy S., Jewhurst V. A., Ellis J. A., Hassard L. E., Clark E. G., Haines D. M., Allan G. M. (1998). Characterization of novel circovirus DNAs associated with wasting syndromes in pigs. J Gen Virol 79, 2171–2179.[PubMed] [Google Scholar]
  31. Morrison D. A. (2010). Using data-display networks for exploratory data analysis in phylogenetic studies. Mol Biol Evol 27, 1044–1057. [View Article][PubMed] [Google Scholar]
  32. Nawagitgul P., Morozov I., Bolin S. R., Harms P. A., Sorden S. D., Paul P. S. (2000). Open reading frame 2 of porcine circovirus type 2 encodes a major capsid protein. J Gen Virol 81, 2281–2287.[PubMed] [Google Scholar]
  33. Olvera A., Cortey M., Segalés J. (2007). Molecular evolution of porcine circovirus type 2 genomes: phylogeny and clonality. Virology 357, 175–185. [View Article][PubMed] [Google Scholar]
  34. Olvera A., Busquets N., Cortey M., de Deus N., Ganges L., Núñez J. I., Peralta B., Toskano J., Dolz R. (2010). Applying phylogenetic analysis to viral livestock diseases: moving beyond molecular typing. Vet J 184, 130–137. [View Article][PubMed] [Google Scholar]
  35. Opriessnig T., Meng X. J., Halbur P. G. (2007). Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J Vet Diagn Invest 19, 591–615. [View Article][PubMed] [Google Scholar]
  36. Opriessnig T., Xiao C. T., Gerber P. F., Halbur P. G. (2013). Emergence of a novel mutant PCV2b variant associated with clinical PCVAD in two vaccinated pig farms in the U.S. concurrently infected with PPV2. Vet Microbiol 163, 177–183. [View Article][PubMed] [Google Scholar]
  37. Patterson A. R., Opriessnig T. (2010). Epidemiology and horizontal transmission of porcine circovirus type 2 (PCV2). Anim Health Res Rev 11, 217–234. [View Article][PubMed] [Google Scholar]
  38. Salgado R. L., Vidigal P. M., de Souza L. F., Onofre T. S., Gonzaga N. F., Eller M. R., Bressan G. C., Fietto J. L., Almeida M. R., Silva Júnior A. (2014). Identification of an emergent porcine circovirus-2 in vaccinated pigs from a Brazilian farm during a postweaning multisystemic wasting syndrome outbreak. Genome Announc 2, e00163–e00114. [View Article][PubMed] [Google Scholar]
  39. Savic B., Milicevic V., Jakic-Dimic D., Bojkovski J., Prodanovic R., Kureljusic B., Potkonjak A. (2012). Genetic characterization and phylogenetic analysis of porcine circovirus type 2 (PCV2) in Serbia. Arch Virol 157, 21–28.[CrossRef] [Google Scholar]
  40. Segalés J., Olvera A., Grau-Roma L., Charreyre C., Nauwynck H., Larsen L., Dupont K., McCullough K., Ellis J. et al. (2008). PCV-2 genotype definition and nomenclature. Vet Rec 162, 867–868. [View Article][PubMed] [Google Scholar]
  41. Segalés J., Kekarainen T., Cortey M. (2013). The natural history of porcine circovirus type 2: from an inoffensive virus to a devastating swine disease?Vet Microbiol 165, 13–20. [View Article][PubMed] [Google Scholar]
  42. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. (2011). mega5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731–2739. [View Article][PubMed] [Google Scholar]
  43. Tischer I., Gelderblom H., Vettermann W., Koch M. A. (1982). A very small porcine virus with circular single-stranded DNA. Nature 295, 64–66. [View Article][PubMed] [Google Scholar]
  44. Trible B. R., Rowland R. R. (2012). Genetic variation of porcine circovirus type 2 (PCV2) and its relevance to vaccination, pathogenesis and diagnosis. Virus Res 164, 68–77. [View Article][PubMed] [Google Scholar]
  45. Turcitu M. A., Wellenberg G. J., Barboi G., Codreanu M. D., Vuta V. B., Nicolae S., Barbuceanu F., Coste H., Cioranu R. (2011). Genetic diversity of porcine circovirus type 2 (PCV2); in the Romanian wild boar population. Res Vet Sci 91, e103–106. [View Article][PubMed] [Google Scholar]
  46. Wang F., Guo X., Ge X., Wang Z., Chen Y., Cha Z., Yang H. (2009). Genetic variation analysis of Chinese strains of porcine circovirus type 2. Virus Res 145, 151–156. [View Article][PubMed] [Google Scholar]
  47. Wei C., Zhang M., Chen Y., Xie J., Huang Z., Zhu W., Xu T., Cao Z., Zhou P. et al. (2013). Genetic evolution and phylogenetic analysis of porcine circovirus type 2 infections in southern China from 2011 to 2012. Infect Genet Evol 17, 87–92. [View Article][PubMed] [Google Scholar]
  48. Xiao C. T., Halbur P. G., Opriessnig T. (2012). Complete genome sequence of a novel porcine circovirus type 2b variant present in cases of vaccine failures in the United States. J Virol 86, 12469. [View Article][PubMed] [Google Scholar]
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Global molecular genetic analysis of porcine circovirus type 2 (PCV2) sequences confirms the presence of four main PCV2 genotypes and reveals a rapid increase of PCV2d
J. Gen. Virol. 96, 1830 (2015); https://doi.org/10.1099/vir.0.000100
/content/journal/jgv/10.1099/vir.0.000100
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