Co-circulation of highly diverse Aleutian mink disease virus strains in Finland Free

Abstract

Aleutian mink disease virus (AMDV) is the causative agent of Aleutian disease (AD), which affects mink of all genotypes and also infects other mustelids such as ferrets, martens and badgers. Previous studies have investigated diversity in Finnish AMDV strains, but these studies have been restricted to small parts of the virus genome, and mostly from newly infected farms and free-ranging mustelids. Here, we investigated the diversity and evolution of Finnish AMDV strains by sequencing the complete coding sequences of 31 strains from mink originating from farms differing in their virus history, as well as from free-ranging mink. The data set was supplemented with partial genomes obtained from 26 strains. The sequences demonstrate that the Finnish AMDV strains have considerable diversity, and that the virus has been introduced to Finland in multiple events. Frequent recombination events were observed, as well as variation in the evolutionary rate in different parts of the genome and between different branches of the phylogenetic tree. Mink in the wild carry viruses with high intra-host diversity and are occasionally even co-infected by two different strains, suggesting that free-ranging mink tolerate chronic infections for extended periods of time. These findings highlight the need for further sampling to understand the mechanisms playing a role in the evolution and pathogenesis of AMDV.

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2018-12-10
2024-03-29
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References

  1. Shahrabadi MS, Cho HJ, Marusyk RG. Characterization of the protein and nucleic acid of Aleutian disease virus. J Virol 1977; 23:353–362[PubMed]
    [Google Scholar]
  2. Bloom ME, Race RE, Wolfinbarger JB. Characterization of Aleutian disease virus as a parvovirus. J Virol 1980; 35:836–843
    [Google Scholar]
  3. Canuti M, Whitney HG, Lang AS. Amdoparvoviruses in small mammals: expanding our understanding of parvovirus diversity, distribution, and pathology. Front Microbiol 2015; 6:1119 [View Article][PubMed]
    [Google Scholar]
  4. Cotmore SF, Agbandje-McKenna M, Chiorini JA, Mukha DV, Pintel DJ et al. The family Parvoviridae. Arch Virol 2014; 159:1239–1247 [View Article][PubMed]
    [Google Scholar]
  5. Bloom ME, Alexandersen S, Perryman S, Lechner D, Wolfinbarger JB. Nucleotide sequence and genomic organization of Aleutian mink disease parvovirus (ADV): sequence comparisons between a nonpathogenic and a pathogenic strain of ADV. J Virol 1988; 62:2903–2915
    [Google Scholar]
  6. Bloom ME, Alexandersen S, Garon CF, Mori S, Wei W et al. Nucleotide sequence of the 5'-terminal palindrome of Aleutian mink disease parvovirus and construction of an infectious molecular clone. J Virol 1990; 64:3551–3556[PubMed]
    [Google Scholar]
  7. Qiu J, Cheng F, Burger LR, Pintel D. The transcription profile of Aleutian mink disease virus in CRFK cells is generated by alternative processing of pre-mRNAs produced from a single promoter. J Virol 2006; 80:654–662
    [Google Scholar]
  8. Qiu J, Cheng F, Pintel D. The abundant R2 mRNA generated by aleutian mink disease parvovirus is tricistronic, encoding NS2, VP1, and VP2. J Virol 2007; 81:6993–7000 [View Article][PubMed]
    [Google Scholar]
  9. Huang Q, Luo Y, Cheng F, Best SM, Bloom ME et al. Molecular characterization of the small nonstructural proteins of parvovirus Aleutian mink disease virus (AMDV) during infection. Virology 2014; 452-453:23–31 [View Article][PubMed]
    [Google Scholar]
  10. Bloom ME, Kanno H, Mori S, Wolfinbarger JB. Aleutian mink disease: puzzles and paradigms Infect . Agents Dis 1994; 3:279–301
    [Google Scholar]
  11. Aasted B. Aleutian disease of mink. Virology and immunology Acta Pathol . Microbiol Immunol Scand Suppl 1985; 287:1–47
    [Google Scholar]
  12. Hussain I, Price GW, Farid AH. Inactivation of Aleutian mink disease virus through high temperature exposure in vitro and under field-based composting conditions. Vet Microbiol 2014; 173:50–58
    [Google Scholar]
  13. Cho HJ. Purification and structure of aleutian disease virus. Front Biol 1976; 44:159–174
    [Google Scholar]
  14. Hartsough GR, Gorham JR. Aleutian disease in mink. Nat Fur News 195610–11
    [Google Scholar]
  15. Gorham J, Henson J, Crawford T, Padgett G. The epizootiology of Aleutian disease; 1976135–158
  16. Knuuttila A, Aronen P, Saarinen A, Vapalahti O. Development and evaluation of an enzyme-linked immunosorbent assay based on recombinant VP2 capsids for the detection of antibodies to Aleutian mink disease virus. Clin Vaccine Immunol 2009; 16:1360–1365 [View Article][PubMed]
    [Google Scholar]
  17. Knuuttila A, Aronen P, Eerola M, Gardner IA, Virtala AM et al. Validation of an automated ELISA system for detection of antibodies to Aleutian mink disease virus using blood samples collected in filter paper strips. Virol J 2014; 11: 141-422X-11-141 [View Article][PubMed]
    [Google Scholar]
  18. Cho HJ, Ingram DG. Antigen and Antibody in Aleutian Disease in Mink. I. Precipitation Reaction by Agar-Gel Electrophoresis. The Journal of Immunology 1972; 108:555–557
    [Google Scholar]
  19. Knuuttila A, Aaltonen K, Virtala AM, Henttonen H, Isomursu M et al. Aleutian mink disease virus in free-ranging mustelids in Finland - a cross-sectional epidemiological and phylogenetic study. J Gen Virol 2015; 96:1423–1435 [View Article][PubMed]
    [Google Scholar]
  20. Farid AH. Aleutian mink disease virus in furbearing mammals in Nova Scotia, Canada. Acta Vet Scand 2013; 55:10-0147–10-0155
    [Google Scholar]
  21. Fournier-Chambrillon C, Aasted B, Perrot A, Pontier D, Sauvage F et al. Antibodies to Aleutian mink disease parvovirus in free-ranging European mink (Mustela lutreola) and other small carnivores from southwestern France. J Wildl Dis 2004; 40:394–402 [View Article][PubMed]
    [Google Scholar]
  22. Murakami M, Matsuba C, Une Y, Nomura Y, Fujitani H. Nucleotide sequence and polymerase chain reaction/restriction fragment length polymorphism analyses of Aleutian disease virus in ferrets in Japan. J Vet Diagn Invest 2001; 13:337–340 [View Article][PubMed]
    [Google Scholar]
  23. Li L, Pesavento PA, Woods L, Clifford DL, Luff J et al. Novel amdovirus in gray foxes. Emerg Infect Dis 2011; 17:1876–1878
    [Google Scholar]
  24. Shao XQ, Wen YJ, Hx B, Zhang XT, Yue ZG et al. Novel amdoparvovirus infecting farmed raccoon dogs and arctic foxes. Emerg Infect Dis 2014; 20:2085–2088
    [Google Scholar]
  25. Bodewes R, Ruiz-Gonzalez A, Schapendonk CM, van den Brand JM, Osterhaus AD et al. Viral metagenomic analysis of feces of wild small carnivores. Virol J 2014; 11: 89-422X-11-89 [View Article][PubMed]
    [Google Scholar]
  26. Canuti M, Doyle HE, P Britton A, Lang AS. Full genetic characterization and epidemiology of a novel amdoparvovirus in striped skunk (Mephitis mephitis). Emerg Microbes Infect 2017; 6:e30 [View Article][PubMed]
    [Google Scholar]
  27. Knuuttila A, Uzcategui N, Kankkonen J, Vapalahti O, Kinnunen P. Molecular epidemiology of Aleutian mink disease virus in Finland. Vet Microbiol 2009; 133:229–238
    [Google Scholar]
  28. Canuti M, O'Leary KE, Hunter BD, Spearman G, Ojkic D et al. Driving forces behind the evolution of the Aleutian mink disease parvovirus in the context of intensive farming. Virus Evol 2016; 2:vew004 [View Article][PubMed]
    [Google Scholar]
  29. Hagberg EE, Krarup A, Fahnøe U, Larsen LE, Dam-Tuxen R et al. A fast and robust method for whole genome sequencing of the Aleutian Mink Disease Virus (AMDV) genome. J Virol Methods 2016; 234:43–51 [View Article][PubMed]
    [Google Scholar]
  30. Hagberg EE, Pedersen AG, Larsen LE, Krarup A. Evolutionary analysis of whole-genome sequences confirms inter-farm transmission of Aleutian mink disease virus. J Gen Virol 2017; 98:1360–1371 [View Article][PubMed]
    [Google Scholar]
  31. Li Y, Huang J, Jia Y, Du Y, Jiang P et al. Genetic characterization of Aleutian mink disease viruses isolated in China. Virus Genes 2012; 45:24–30 [View Article][PubMed]
    [Google Scholar]
  32. van Dawen S, Kaaden OR, Roth S. Propagation of Aleutian disease parvovirus in cell line CCC clone 81. Arch Virol 1983; 77:39–50 [View Article][PubMed]
    [Google Scholar]
  33. Xi J, Wang J, Yu Y, Zhang X, Mao Y et al. Genetic characterization of the complete genome of an Aleutian mink disease virus isolated in north China. Virus Genes 2016; 52:463–473 [View Article][PubMed]
    [Google Scholar]
  34. Ryt-Hansen P, Hagberg EE, Chriél M, Struve T, Pedersen AG et al. Global phylogenetic analysis of contemporary aleutian mink disease viruses (AMDVs). Virol J 2017; 14: 231-017-0898-y [View Article][PubMed]
    [Google Scholar]
  35. Suomen Turkiseläinten Kasvattajain Liitto (STKL).. Suomen Turkiseläinten Kasvattajain Liitto (STKL). https://profur.fi/
  36. Nes N, Einarsson E, Lohi O, Jørgensen G. Beautiful fur animals – and their colour genetics1988.
  37. Nummi P. Suomeen istutetut riistaeläimet. Helsingin yliopisto, Maatalous- ja Metsäeläintieteen Laitos 198813–15
    [Google Scholar]
  38. Jakubczak A, Kowalczyk M, Kostro K, Jezewska-Witkowska G. Comparative molecular analysis of strains of the Aleutian Disease Virus isolated from farmed and wild mink. Ann Agric Environ Med 2017; 24:366–371 [View Article][PubMed]
    [Google Scholar]
  39. Hoelzer K, Shackelton LA, Holmes EC, Parrish CR. Within-host genetic diversity of endemic and emerging parvoviruses of dogs and cats. J Virol 2008; 82:11096–11105 [View Article][PubMed]
    [Google Scholar]
  40. Shackelton LA, Hoelzer K, Parrish CR, Holmes EC. Comparative analysis reveals frequent recombination in the parvoviruses. J Gen Virol 2007; 88:3294–3301 [View Article][PubMed]
    [Google Scholar]
  41. Ohshima T, Mochizuki M. Evidence for recombination between feline panleukopenia virus and canine parvovirus type 2. J Vet Med Sci 2009; 71:403–408 [View Article][PubMed]
    [Google Scholar]
  42. Wang J, Cheng S, Yi L, Cheng Y, Yang S et al. Evidence for natural recombination between mink enteritis virus and canine parvovirus. Virol J 2012; 9:252–259 [View Article][PubMed]
    [Google Scholar]
  43. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008; 9:267–276 [View Article][PubMed]
    [Google Scholar]
  44. Hoelzer K, Shackelton LA, Parrish CR, Holmes EC. Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. J Gen Virol 2008; 89:2280–2289 [View Article][PubMed]
    [Google Scholar]
  45. Hoelzer K, Parrish CR. The emergence of parvoviruses of carnivores. Vet Res 2010; 41:39 [View Article][PubMed]
    [Google Scholar]
  46. Shackelton LA, Parrish CR, Truyen U, Holmes EC. High rate of viral evolution associated with the emergence of carnivore parvovirusProc . Natl Acad Sci USA 2005; 102:379–384 [View Article]
    [Google Scholar]
  47. Jensen TH, Christensen LS, Chriél M, Uttenthal A, Hammer AS. Implementation and validation of a sensitive PCR detection method in the eradication campaign against Aleutian mink disease virus. J Virol Methods 2011; 171:81–85 [View Article][PubMed]
    [Google Scholar]
  48. Okonechnikov K, Golosova O, Fursov M. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 2012; 28:1166–1167 [View Article][PubMed]
    [Google Scholar]
  49. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article][PubMed]
    [Google Scholar]
  50. Li H. Aligning sequence reads, clone sequences and assembly contigs with. BWA-MEM2013. arXiv:1303.3997
  51. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  52. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS et al. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 1999; 73:152–160
    [Google Scholar]
  53. Simmonds P. SSE: a nucleotide and amino acid sequence analysis platform. BMC Res Notes 2012; 5: 50-0500-5-50 [View Article][PubMed]
    [Google Scholar]
  54. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  55. Rambaut A, Suchard M, Xie D, Drummond A. Tracer v1.6; 2014; 6 http://tree.bio.ed.ac.uk/software/tracer/
  56. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA et al. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty Mol . Biol Evol 2012; 29:2157–2167
    [Google Scholar]
  57. Baele G, Wl L, Drummond AJ, Suchard MA, Lemey P. Accurate model selection of relaxed molecular clocks in bayesian phylogenetics. Mol Biol Evol 2013; 30:239–243
    [Google Scholar]
  58. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000; 16:562–563 [View Article][PubMed]
    [Google Scholar]
  59. Padidam M, Sawyer S, Fauquet CM. Possible emergence of new geminiviruses by frequent recombination. Virology 1999; 265:218–225 [View Article][PubMed]
    [Google Scholar]
  60. Salminen MO, Carr JK, Burke DS, McCutchan FE. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 1995; 11:1423–1425 [View Article][PubMed]
    [Google Scholar]
  61. Smith JM. Analyzing the mosaic structure of genes. J Mol Evol 1992; 34:126–129 [View Article][PubMed]
    [Google Scholar]
  62. Posada D, Crandall KA. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 2001; 98:13757–13762 [View Article][PubMed]
    [Google Scholar]
  63. Gibbs MJ, Armstrong JS, Gibbs AJ. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000; 16:573–582 [View Article][PubMed]
    [Google Scholar]
  64. Boni MF, Posada D, Feldman MW. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007; 176:1035–1047 [View Article][PubMed]
    [Google Scholar]
  65. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:vev003 [View Article][PubMed]
    [Google Scholar]
  66. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  67. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  68. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011; 27:2987–2993 [View Article][PubMed]
    [Google Scholar]
  69. Wilm A, Aw PP, Bertrand D, Yeo GH, Ong SH et al. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res 2012; 40:11189–11201 [View Article][PubMed]
    [Google Scholar]
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