1887

Abstract

A detailed analysis of the Ns1/Vp1Vp2 genome region of the porcine parvovirus (PPV) strains isolated from vaccinated animals was performed. We found many inconsistencies in the phylogenetic trees of these viral isolates, such as low statistical support and strains with long branches in the phylogenetic trees. Thus, we used distance-based and phylogenetic methods to distinguish recombinants from spurious recombination signals. We found a mosaic virus in which the gene was acquired from one PPV clade and the gene was acquired from a distinct phylogenetic clade. We also described the interclade mosaic structure of the gene of a reference strain. If recombination is an adaptive mechanism over the course of PPV evolution, we would likely observe increasing numbers of chimeric strains over time. However, when the PPV sequences isolated from 1964 to 2011 were analysed, only two chimeric strains were detected. Thus, PPV recombination is an independent event, resulting from close contact between animals housed in high-density conditions.

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2012-12-01
2021-10-18
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References

  1. Abe K., Kiuchi T., Tanaka K., Edamoto Y., Aiba N., Sata T. 2007; Characterization of erythrovirus B19 genomes isolated in liver tissues from patients with fulminant hepatitis and biliary atresia who underwent liver transplantation. Int J Med Sci 4:105–109 [View Article][PubMed]
    [Google Scholar]
  2. Ané C. 2011; Detecting phylogenetic breakpoints and discordance from genome-wide alignments for species tree reconstruction. Genome Biol Evol 3:246–258 [View Article][PubMed]
    [Google Scholar]
  3. Awadalla P. 2003; The evolutionary genomics of pathogen recombination. Nat Rev Genet 4:50–60 [View Article][PubMed]
    [Google Scholar]
  4. Bartosch B., Stefanidis D., Myers R., Weiss R., Patience C., Takeuchi Y. 2004; Evidence and consequence of porcine endogenous retrovirus recombination. J Virol 78:13880–13890 [View Article][PubMed]
    [Google Scholar]
  5. Bay R. A., Bielawski J. P. 2011; Recombination detection under evolutionary scenarios relevant to functional divergence. J Mol Evol 73:273–286[PubMed] [CrossRef]
    [Google Scholar]
  6. Boni M. F., Posada D., Feldman M. W. 2007; An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047 [View Article][PubMed]
    [Google Scholar]
  7. Cadar D., Cságola A., Lorincz M., Tombácz K., Spînu M., Tuboly T. 2012; Detection of natural inter- and intra-genotype recombination events revealed by cap gene analysis and decreasing prevalence of PCV2 in wild boars. Infect Genet Evol 12:420–427 [View Article][PubMed]
    [Google Scholar]
  8. Cheng W., Chen J., Xu Z., Yu J., Huang C., Jin M., Li H., Zhang M., Jin Y., Duan Z. J. 2011; Phylogenetic and recombination analysis of human bocavirus 2. BMC Infect Dis 11:50 [View Article][PubMed]
    [Google Scholar]
  9. Christensen J., Tattersall P. 2002; Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J Virol 76:6518–6531 [View Article][PubMed]
    [Google Scholar]
  10. Cotmore S. F., Tattersall P. 1998; High-mobility group 1/2 proteins are essential for initiating rolling-circle-type DNA replication at a parvovirus hairpin origin. J Virol 72:8477–8484[PubMed]
    [Google Scholar]
  11. Crotty S., Maag D., Arnold J. J., Zhong W., Lau J. Y., Hong Z., Andino R., Cameron C. E. 2000; The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nat Med 6:1375–1379 [View Article][PubMed]
    [Google Scholar]
  12. Cságola A., Lőrincz M., Cadar D., Tombácz K., Biksi I., Tuboly T. 2012; Detection, prevalence and analysis of emerging porcine parvovirus infections. Arch Virol 157:1003–1010 [View Article][PubMed]
    [Google Scholar]
  13. Etherington G. J., Dicks J., Roberts I. N. 2005; Recombination analysis tool (RAT): a program for the high-throughput detection of recombination. Bioinformatics 21:278–281 [View Article][PubMed]
    [Google Scholar]
  14. Grigoras I., Timchenko T., Grande-Pérez A., Katul L., Vetten H. J., Gronenborn B. 2010; High variability and rapid evolution of a nanovirus. J Virol 84:9105–9117 [View Article][PubMed]
    [Google Scholar]
  15. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  16. Hasegawa M., Kishino H., Yano T. 1985; Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174 [View Article][PubMed]
    [Google Scholar]
  17. Hogan A., Faust E. A. 1986; Nonhomologous recombination in the parvovirus chromosome: role for a CTATTTCT motif. Mol Cell Biol 6:3005–3009[PubMed]
    [Google Scholar]
  18. Hughes M. L., Poon R., Adams V., Sayeed S., Saputo J., Uzal F. A., McClane B. A., Rood J. I. 2007; Epsilon-toxin plasmids of Clostridium perfringens type D are conjugative. J Bacteriol 189:7531–7538 [View Article][PubMed]
    [Google Scholar]
  19. Husmeier D., Mantzaris A. V. 2008; Addressing the shortcomings of three recent Bayesian methods for detecting interspecific recombination in DNA sequence alignments. Stat Appl Genet Mol Biol 7:34[PubMed]
    [Google Scholar]
  20. Huson D. H., Bryant D. 2006; Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267 [View Article][PubMed]
    [Google Scholar]
  21. Jayaraman A., Pappas C., Raman R., Belser J. A., Viswanathan K., Shriver Z., Tumpey T. M., Sasisekharan R. 2011; A single base-pair change in 2009 H1N1 hemagglutinin increases human receptor affinity and leads to efficient airborne viral transmission in ferrets. PLoS ONE 6:e17616 [View Article][PubMed]
    [Google Scholar]
  22. Kaneko H., Aoki K., Ishida S., Ohno S., Kitaichi N., Ishiko H., Fujimoto T., Ikeda Y., Nakamura M. other authors 2011; Recombination analysis of intermediate human adenovirus type 53 in Japan by complete genome sequence. J Gen Virol 92:1251–1259 [View Article][PubMed]
    [Google Scholar]
  23. Kapoor A., Simmonds P., Slikas E., Li L., Bodhidatta L., Sethabutr O., Triki H., Bahri O., Oderinde B. S. other authors 2010; Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J Infect Dis 201:1633–1643 [View Article][PubMed]
    [Google Scholar]
  24. Kellam P., Larder B. A. 1995; Retroviral recombination can lead to linkage of reverse transcriptase mutations that confer increased zidovudine resistance. J Virol 69:669–674[PubMed]
    [Google Scholar]
  25. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D. 2006; Gard: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098 [View Article][PubMed]
    [Google Scholar]
  26. Kresse J. I., Taylor W. D., Stewart W. W., Eernisse K. A. 1985; Parvovirus infection in pigs with necrotic and vesicle-like lesions. Vet Microbiol 10:525–531 [View Article][PubMed]
    [Google Scholar]
  27. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. other authors 2007; clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  28. Lauring A. S., Andino R. 2010; Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 6:e1001005 [View Article][PubMed]
    [Google Scholar]
  29. Leal E., Villanova F. E. 2010; Diversity of HIV-1 subtype B: implications to the origin of BF recombinants. PLoS ONE 5:e11833 [View Article][PubMed]
    [Google Scholar]
  30. Leitner T., Albert J. 1999; The molecular clock of HIV-1 unveiled through analysis of a known transmission history. Proc Natl Acad Sci U S A 96:10752–10757 [View Article][PubMed]
    [Google Scholar]
  31. López-Bueno A., Villarreal L. P., Almendral J. M. 2006; Parvovirus variation for disease: a difference with RNA viruses?. Curr Top Microbiol Immunol 299:349–370 [View Article][PubMed]
    [Google Scholar]
  32. Lukashov V. V., Goudsmit J. 2001; Evolutionary relationships among parvoviruses: virus-host coevolution among autonomous primate parvoviruses and links between adeno-associated and avian parvoviruses. J Virol 75:2729–2740 [View Article][PubMed]
    [Google Scholar]
  33. Margeridon-Thermet S., Shafer R. W. 2010; Comparison of the mechanisms of drug resistance among HIV, hepatitis B, and hepatitis C. Viruses 2:2696–2739 [View Article][PubMed]
    [Google Scholar]
  34. Martin D. P., Williamson C., Posada D. 2005; RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262 [View Article][PubMed]
    [Google Scholar]
  35. Martin D. P., Biagini P., Lefeuvre P., Golden M., Roumagnac P., Varsani A. 2011; Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738 [View Article][PubMed]
    [Google Scholar]
  36. Martins L. O., Leal E., Kishino H. 2008; Phylogenetic detection of recombination with a Bayesian prior on the distance between trees. PLoS ONE 3:e2651 [View Article][PubMed]
    [Google Scholar]
  37. Maydt J., Lengauer T. 2006; Recco: recombination analysis using cost optimization. Bioinformatics 22:1064–1071 [View Article][PubMed]
    [Google Scholar]
  38. McClurkin A. W., Norman J. O. 1966; Studies on transmissible gastroenteritis of swine. II. Selected characteristics of a cytopathogenic virus common to five isolates from transmissible gastroenteritis. Can J Comp Med Vet Sci 30:190–198[PubMed]
    [Google Scholar]
  39. Mengeling W. L. 2006; Porcine parvovirus. In Diseases of swine, 9th edn. Edited by Straw E. B. Z., D’Allaire S., Taylor D., Ames D. J. Iowa: Blackwell Publishing/Iowa University Press;
    [Google Scholar]
  40. Mild M., Esbjörnsson J., Fenyö E. M., Medstrand P. 2007; Frequent intrapatient recombination between human immunodeficiency virus type 1 R5 and X4 envelopes: implications for coreceptor switch. J Virol 81:3369–3376 [View Article][PubMed]
    [Google Scholar]
  41. Milne I., Wright F., Rowe G., Marshall D. F., Husmeier D., McGuire G. 2004; TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20:1806–1807 [View Article][PubMed]
    [Google Scholar]
  42. Mochizuki M., Ohshima T., Une Y., Yachi A. 2008; Recombination between vaccine and field strains of canine parvovirus is revealed by isolation of virus in canine and feline cell cultures. J Vet Med Sci 70:1305–1314 [View Article][PubMed]
    [Google Scholar]
  43. Moutouh L., Corbeil J., Richman D. D. 1996; Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proc Natl Acad Sci U S A 93:6106–6111 [View Article][PubMed]
    [Google Scholar]
  44. Noppornpanth S., Lien T. X., Poovorawan Y., Smits S. L., Osterhaus A. D., Haagmans B. L. 2006; Identification of a naturally occurring recombinant genotype 2/6 hepatitis C virus. J Virol 80:7569–7577 [View Article][PubMed]
    [Google Scholar]
  45. Nora T., Charpentier C., Tenaillon O., Hoede C., Clavel F., Hance A. J. 2007; Contribution of recombination to the evolution of human immunodeficiency viruses expressing resistance to antiretroviral treatment. J Virol 81:7620–7628 [View Article][PubMed]
    [Google Scholar]
  46. Norberg P., Kasubi M. J., Haarr L., Bergström T., Liljeqvist J. A. 2007; Divergence and recombination of clinical herpes simplex virus type 2 isolates. J Virol 81:13158–13167 [View Article][PubMed]
    [Google Scholar]
  47. Norja P., Eis-Hübinger A. M., Söderlund-Venermo M., Hedman K., Simmonds P. 2008; Rapid sequence change and geographical spread of human parvovirus B19: comparison of B19 virus evolution in acute and persistent infections. J Virol 82:6427–6433 [View Article][PubMed]
    [Google Scholar]
  48. Ohshima T., Mochizuki M. 2009; Evidence for recombination between feline panleukopenia virus and canine parvovirus type 2. J Vet Med Sci 71:403–408 [View Article][PubMed]
    [Google Scholar]
  49. Oraveerakul K., Choi C. S., Molitor T. W. 1992; Restriction of porcine parvovirus replication in nonpermissive cells. J Virol 66:715–722[PubMed]
    [Google Scholar]
  50. Papke R. T., Zhaxybayeva O., Feil E. J., Sommerfeld K., Muise D., Doolittle W. F. 2007; Searching for species in haloarchaea. Proc Natl Acad Sci U S A 104:14092–14097 [View Article][PubMed]
    [Google Scholar]
  51. Pereira C. A., Leal E. S., Durigon E. L. 2007; Selective regimen shift and demographic growth increase associated with the emergence of high-fitness variants of canine parvovirus. Infect Genet Evol 7:399–409 [View Article][PubMed]
    [Google Scholar]
  52. Posada D. 2002; Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717 [View Article][PubMed]
    [Google Scholar]
  53. Posada D. 2008; jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256 [View Article][PubMed]
    [Google Scholar]
  54. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [View Article][PubMed]
    [Google Scholar]
  55. Rambaut A., Posada D., Crandall K. A., Holmes E. C. 2004; The causes and consequences of HIV evolution. Nat Rev Genet 5:52–61 [View Article][PubMed]
    [Google Scholar]
  56. Rousseau C. M., Learn G. H., Bhattacharya T., Nickle D. C., Heckerman D., Chetty S., Brander C., Goulder P. J., Walker B. D. other authors 2007; Extensive intrasubtype recombination in South African human immunodeficiency virus type 1 subtype C infections. J Virol 81:4492–4500 [View Article][PubMed]
    [Google Scholar]
  57. Sanjuán R., Nebot M. R., Chirico N., Mansky L. M., Belshaw R. 2010; Viral mutation rates. J Virol 84:9733–9748 [View Article][PubMed]
    [Google Scholar]
  58. Sawyer S. 1989; Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538[PubMed]
    [Google Scholar]
  59. Schierup M. H., Mordhorst C. H., Muller C. P., Christensen L. S. 2005; Evidence of recombination among early-vaccination era measles virus strains. BMC Evol Biol 5:52 [View Article][PubMed]
    [Google Scholar]
  60. Schultz A. K., Zhang M., Leitner T., Kuiken C., Korber B., Morgenstern B., Stanke M. 2006; A jumping profile Hidden Markov Model and applications to recombination sites in HIV and HCV genomes. BMC Bioinformatics 7:265 [View Article][PubMed]
    [Google Scholar]
  61. Shackelton L. A., Holmes E. C. 2006; Phylogenetic evidence for the rapid evolution of human B19 erythrovirus. J Virol 80:3666–3669 [View Article][PubMed]
    [Google Scholar]
  62. Shackelton L. A., Hoelzer K., Parrish C. R., Holmes E. C. 2007; Comparative analysis reveals frequent recombination in the parvoviruses. J Gen Virol 88:3294–3301 [View Article][PubMed]
    [Google Scholar]
  63. Shangjin C., Cortey M., Segalés J. 2009; Phylogeny and evolution of the NS1 and VP1/VP2 gene sequences from porcine parvovirus. Virus Res 140:209–215 [View Article][PubMed]
    [Google Scholar]
  64. Smith J. M. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129 [View Article][PubMed]
    [Google Scholar]
  65. Stainton D., Kraberger S., Walters M., Wiltshire E. J., Rosario K., Halafihi M., Lolohea S., Katoa I., Faitua T. H. other authors 2012; Evidence of inter-component recombination, intra-component recombination and reassortment in banana bunchy top virus. J Gen Virol 93:1103–1119 [View Article][PubMed]
    [Google Scholar]
  66. Streck A. F., Bonatto S. L., Homeier T., Souza C. K., Gonçalves K. R., Gava D., Canal C. W., Truyen U. 2011; High rate of viral evolution in the capsid protein of porcine parvovirus. J Gen Virol 92:2628–2636 [View Article][PubMed]
    [Google Scholar]
  67. Suryavanshi G. W., Dixit N. M. 2007; Emergence of recombinant forms of HIV: dynamics and scaling. PLOS Comput Biol 3:2003–2018 [View Article][PubMed]
    [Google Scholar]
  68. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  69. Westesson O., Holmes I. 2009; Accurate detection of recombinant breakpoints in whole-genome alignments. PLOS Comput Biol 5:e1000318 [View Article][PubMed]
    [Google Scholar]
  70. Wiuf C., Christensen T., Hein J. 2001; A simulation study of the reliability of recombination detection methods. Mol Biol Evol 18:1929–1939 [View Article][PubMed]
    [Google Scholar]
  71. Worobey M., Holmes E. C. 2001; Homologous recombination in GB virus C/hepatitis G virus. Mol Biol Evol 18:254–261 [View Article][PubMed]
    [Google Scholar]
  72. Zeeuw E. J., Leinecker N., Herwig V., Selbitz H. J., Truyen U. 2007; Study of the virulence and cross-neutralization capability of recent porcine parvovirus field isolates and vaccine viruses in experimentally infected pregnant gilts. J Gen Virol 88:420–427 [View Article][PubMed]
    [Google Scholar]
  73. Zell R., Taudien S., Pfaff F., Wutzler P., Platzer M., Sauerbrei A. 2012; Sequencing of 21 varicella-zoster virus genomes reveals two novel genotypes and evidence of recombination. J Virol 86:1608–1622 [View Article][PubMed]
    [Google Scholar]
  74. Zimmermann P., Ritzmann M., Selbitz H. J., Heinritzi K., Truyen U. 2006; VP1 sequences of German porcine parvovirus isolates define two genetic lineages. J Gen Virol 87:295–301 [View Article][PubMed]
    [Google Scholar]
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