1887

Abstract

Bovine viral diarrhoea (BVD) is an important disease of cattle, with significant impacts on animal health and welfare. The wide host range of the causative pestiviruses may lead to formation of virus reservoirs in other ruminant or wildlife species, presenting a concern for the long-term success of BVD eradication campaigns. It is likely that the quasispecies nature of these RNA viruses contributes to their interspecies transmission by providing genetic plasticity. Understanding the spectrum of sequence variants present in persistently infected (PI) animals is, therefore, essential for studies of virus transmission. To analyse quasispecies diversity without amplification bias, we extracted viral RNA from the serum of a PI cow, and from cell culture fluid after three passages of the same virus in culture, to produce cDNA without amplification. Sequencing of this material using Illumina 250 bp paired-read technology produced full-length virus consensus sequences from both sources and demonstrated the quasispecies diversity of this pestivirus A genotype 1a field strain within serum and after culture. We report the distribution and diversity of over 800 SNPs and provide evidence for a loss of diversity after only three passages in cell culture, implying that cultured viruses cannot be used to understand quasispecies diversity and may not provide reliable molecular markers for source tracing or transmission studies. Additionally, both serum and cultured viruses could be sequenced as a set of 25 overlapping PCR amplicons that demonstrated the same consensus sequences and the presence of many of the same quasispecies variants. The observation that aspects of the quasispecies structure revealed by massively parallel sequencing are also detected after PCR and Sanger sequencing suggests that this approach may be useful for small or difficult to analyse samples.

Funding
This study was supported by the:
  • George C Russell , Rural and Environment Science and Analytical Services Division , (Award EPIC3)
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000343
2020-03-11
2020-06-03
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/4/mgen000343.html?itemId=/content/journal/mgen/10.1099/mgen.0.000343&mimeType=html&fmt=ahah

References

  1. Peterhans E, Schweizer M. BVDV: a pestivirus inducing tolerance of the innate immune response. Biologicals 2013; 41:39–51 [CrossRef]
    [Google Scholar]
  2. Eigen M, Schuster P. The hypercycle. A principle of natural self-organization. Part A: emergence of the hypercycle. Naturwissenschaften 1977; 64:541–565 [CrossRef]
    [Google Scholar]
  3. Andino R, Domingo E. Viral quasispecies. Virology 2015; 479-480:46–51 [CrossRef]
    [Google Scholar]
  4. Booth RE, Thomas CJ, El-Attar LMR, Gunn G, Brownlie J. A phylogenetic analysis of bovine viral diarrhoea virus (BVDV) isolates from six different regions of the UK and links to animal movement data. Vet Res 2013; 44:43 [CrossRef]
    [Google Scholar]
  5. Courtenay AE, Henderson RG, Cranwell MP, Sandvik T. BVD virus type 2 infection and severe clinical disease in a dairy herd. Vet Rec 2007; 160:706–707 [CrossRef]
    [Google Scholar]
  6. Smith DB, Meyers G, Bukh J, Gould EA, Monath T et al. Proposed revision to the taxonomy of the genus Pestivirus, family Flaviviridae . J Gen Virol 2017; 98:2106–2112 [CrossRef]
    [Google Scholar]
  7. Vilcek S, Durkovic B, Kolesarova M, Paton DJ. Genetic diversity of BVDV: consequences for classification and molecular epidemiology. Prev Vet Med 2005; 72:31–35 [CrossRef]
    [Google Scholar]
  8. Vilcek S, Paton DJ, Durkovic B, Strojny L, Ibata G et al. Bovine viral diarrhoea virus genotype 1 can be separated into at least eleven genetic groups. Arch Virol 2001; 146:99–115 [CrossRef]
    [Google Scholar]
  9. Yeşilbağ K, Alpay G, Becher P. Variability and global distribution of subgenotypes of bovine viral diarrhea virus. Viruses 2017; 9:128 [CrossRef]
    [Google Scholar]
  10. Bazzucchi M, Bertolotti L, Giammarioli M, Rossi E, Petrini S et al. Complete genome sequence of a bovine viral diarrhea virus subgenotype 1G strain isolated in Italy. Genome Announc 2017; 5:e00263-17 [CrossRef]
    [Google Scholar]
  11. Nettleton PF, Herring JA, Corrigall W. Isolation of bovine virus diarrhoea virus from a Scottish red deer. Vet Rec 1980; 107:425–426 [CrossRef]
    [Google Scholar]
  12. Fernández-Aguilar X, López-Olvera JR, Marco I, Rosell R, Colom-Cadena A et al. Pestivirus in alpine wild ruminants and sympatric livestock from the Cantabrian Mountains, Spain. Vet Rec 2016; 178:586 [CrossRef]
    [Google Scholar]
  13. Frolich K, Thiede S, Kozikowski T, Jakob W. A review of mutual transmission of important infectious diseases between livestock and wildlife in Europe. Ann N Y Acad Sci 2002; 969:4–13 [CrossRef]
    [Google Scholar]
  14. Ridpath JF, Neill JD. Challenges in identifying and determining the impacts of infection with pestiviruses on the herd health of free ranging cervid populations. Front Microbiol 2016; 7:921 [CrossRef]
    [Google Scholar]
  15. Deng Y, Sun C-Q, Cao S-J, Lin T, Yuan S-S et al. High prevalence of bovine viral diarrhea virus 1 in Chinese swine herds. Vet Microbiol 2012; 159:490–493 [CrossRef]
    [Google Scholar]
  16. Tao J, Liao J, Wang Y, Zhang X, Wang J et al. Bovine viral diarrhea virus (BVDV) infections in pigs. Vet Microbiol 2013; 165:185–189 [CrossRef]
    [Google Scholar]
  17. Chakraborty AK, Mukherjee P, Karam A, Das S, Barkalita L et al. Evidence of BVDV in pigs from North Eastern part of India - genetic profiling and characterisation. Open Virol J 2018; 12:110–120 [CrossRef]
    [Google Scholar]
  18. Rossmanith W, Jacková A, Appel F, Wilhelm E, Vilcek S. Analysis of BVDV isolates and factors contributing to virus transmission in the final stage of a BVDV eradication program in lower Austria. Berl Munch Tierarztl Wochenschr 2014; 127:12–18
    [Google Scholar]
  19. Ståhl K, Kampa J, Baule C, Isaksson M, Moreno-López J et al. Molecular epidemiology of bovine viral diarrhoea during the final phase of the Swedish BVD-eradication programme. Prev Vet Med 2005; 72:103–108 [CrossRef]
    [Google Scholar]
  20. Stalder H, Hug C, Zanoni R, Vogt H-R, Peterhans E et al. A nationwide database linking information on the hosts with sequence data of their virus strains: a useful tool for the eradication of bovine viral diarrhea (BVD) in Switzerland. Virus Res 2016; 218:49–56 [CrossRef]
    [Google Scholar]
  21. Giangaspero M, Yesilbag K, Apicella C. Who's who in the bovine viral diarrhea virus type 1 species: genotypes L and R. Virus Res 2018; 256:50–75 [CrossRef]
    [Google Scholar]
  22. Paton D, Gunn M, Sands J, Yapp F, Drew T et al. Establishment of serial persistent infections with bovine viral diarrhoea virus in cattle and sheep and changes in epitope expression related to host species. Arch Virol 1997; 142:929–938 [CrossRef]
    [Google Scholar]
  23. Bachofen C, Vogt H-R, Stalder H, Mathys T, Zanoni R et al. Persistent infections after natural transmission of bovine viral diarrhoea virus from cattle to goats and among goats. Vet Res 2013; 44:15 [CrossRef]
    [Google Scholar]
  24. Kuca T, Passler T, Newcomer BW, Neill JD, Galik PK et al. Identification of conserved amino acid substitutions during serial infection of pregnant cattle and sheep with bovine viral diarrhea virus. Front Microbiol 2018; 9:1109 [CrossRef]
    [Google Scholar]
  25. Meier P. Studies on the molecular evolution of bovine viral diarrhea virus (BVDV). Thesis University of Bern; 1998
    [Google Scholar]
  26. Deng R, Brock KV. Molecular cloning and nucleotide sequence of a pestivirus genome, noncytopathic bovine viral diarrhea virus strain SD-1. Virology 1992; 191:867–879 [CrossRef]
    [Google Scholar]
  27. De Moerlooze L, Lecomte C, Brown-Shimmer S, Schmetz D, Guiot C et al. Nucleotide sequence of the bovine viral diarrhoea virus Osloss strain: comparison with related viruses and identification of specific DNA probes in the 5' untranslated region. J Gen Virol 1993; 74:1433–1438 [CrossRef]
    [Google Scholar]
  28. Meyers G, Tautz N, Becher P, Thiel HJ, Kümmerer BM. Recovery of cytopathogenic and noncytopathogenic bovine viral diarrhea viruses from cDNA constructs. J Virol 1996; 70:8606–8613 [CrossRef]
    [Google Scholar]
  29. Colett MS, Larson R, Gold C, Strick D, Anderson DK et al. Molecular cloning and nucleotide sequence of the pestivirus bovine viral diarrhea virus. Virology 1988; 165:191–199 [CrossRef]
    [Google Scholar]
  30. Xie Z, Fan Q, Xie Z, Liu J, Pang Y et al. Complete genome sequence of a bovine viral diarrhea virus strain isolated in southern China. Genome Announc 2014; 2:e00512-14 [CrossRef]
    [Google Scholar]
  31. Oem J-K, Joo S-K, An D-J. Complete genome sequences of two bovine viral diarrhea viruses isolated from brain tissues of nonambulatory (downer) cattle. Genome Announc 2013; 1:e00733-13 [CrossRef]
    [Google Scholar]
  32. Gao S, Du J, Shao J, Lang Y, Lin T et al. Genome analysis reveals a novel genetically divergent subgenotype of bovine viral diarrhea virus in China. Infect Genet Evol 2014; 21:489–491 [CrossRef]
    [Google Scholar]
  33. Soltan MA, Wilkes RP, Elsheery MN, Elhaig MM, Riley MC et al. Complete genome sequence of bovine viral diarrhea virus-1 strain Egy/Ismailia/2014, subtype 1B. Genome Announc 2015; 3:e01518-15 [CrossRef]
    [Google Scholar]
  34. Stalder H, Schweizer M, Bachofen C. Complete genome sequence of a bovine viral diarrhea virus subgenotype 1E strain isolated in Switzerland. Genome Announc 2015; 3:e00636-15 [CrossRef]
    [Google Scholar]
  35. Workman AM, Harhay GP, Heaton MP, Grotelueschen DM, Sjeklocha D et al. Full-length coding sequences for 12 bovine viral diarrhea virus isolates from persistently infected cattle in a feedyard in Kansas. Genome Announc 2015; 3:e00487-15 [CrossRef]
    [Google Scholar]
  36. Workman AM, Heaton MP, Harhay GP, Smith TPL, Grotelueschen DM et al. Resolving bovine viral diarrhea virus subtypes from persistently infected U.S. beef calves with complete genome sequence. J Vet Diagn Invest 2016; 28:519–528 [CrossRef]
    [Google Scholar]
  37. Neill JD, Bayles DO, Ridpath JF. Simultaneous rapid sequencing of multiple RNA virus genomes. J Virol Methods 2014; 201:68–72 [CrossRef]
    [Google Scholar]
  38. Neill JD, Newcomer BW, Marley SD, Ridpath JF, Givens MD. Genetic change in the open reading frame of bovine viral diarrhea virus is introduced more rapidly during the establishment of a single persistent infection than from multiple acute infections. Virus Res 2011; 158:140–145 [CrossRef]
    [Google Scholar]
  39. Neill JD, Newcomer BW, Marley SD, Ridpath JF, Givens MD. Greater numbers of nucleotide substitutions are introduced into the genomic RNA of bovine viral diarrhea virus during acute infections of pregnant cattle than of non-pregnant cattle. Virol J 2012; 9:150 [CrossRef]
    [Google Scholar]
  40. Neill JD, Workman AM, Hesse R, Bai J, Porter EP et al. Identification of BVDV2b and 2c subgenotypes in the United States: genetic and antigenic characterization. Virology 2019; 528:19–29 [CrossRef]
    [Google Scholar]
  41. Sato A, Tateishi K, Shinohara M, Naoi Y, Shiokawa M et al. Complete genome sequencing of bovine viral diarrhea virus 1, subgenotypes 1n and 1o. Genome Announc 2016; 4:e01744-15 [CrossRef]
    [Google Scholar]
  42. Jenckel M, Höper D, Schirrmeier H, Reimann I, Goller KV et al. Mixed triple: allied viruses in unique recent isolates of highly virulent type 2 bovine viral diarrhea virus detected by deep sequencing. J Virol 2014; 88:6983–6992 [CrossRef]
    [Google Scholar]
  43. Russell GC, Grant DM, Lycett S, Bachofen C, Caldow GL et al. Analysis of bovine viral diarrhoea virus: Biobank and sequence database to support eradication in Scotland. Vet Rec 2017; 180:447 [CrossRef]
    [Google Scholar]
  44. Bachofen C, Grant DM, Willoughby K, Zadoks RN, Dagleish MP et al. Experimental infection of rabbits with bovine viral diarrhoea virus by a natural route of exposure. Vet Res 2014; 45:34 [CrossRef]
    [Google Scholar]
  45. Willoughby K, Valdazo-González B, Maley M, Gilray J, Nettleton PF. Development of a real time RT-PCR to detect and type ovine pestiviruses. J Virol Methods 2006; 132:187–194 [CrossRef]
    [Google Scholar]
  46. Thonur L, Maley M, Gilray J, Crook T, Laming E et al. One-step multiplex real time RT-PCR for the detection of bovine respiratory syncytial virus, bovine herpesvirus 1 and bovine parainfluenza virus 3. BMC Vet Res 2012; 8:9 [CrossRef]
    [Google Scholar]
  47. Vilcek S, Paton D, Lowings P, Björklund H, Nettleton P et al. Genetic analysis of pestiviruses at the 3' end of the genome. Virus Genes 1999; 18:107–114 [CrossRef]
    [Google Scholar]
  48. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [CrossRef]
    [Google Scholar]
  49. Milani A, Fusaro A, Bonfante F, Zamperin G, Salviato A et al. Vaccine immune pressure influences viral population complexity of avian influenza virus during infection. Vet Microbiol 2017; 203:88–94 [CrossRef]
    [Google Scholar]
  50. Yoon H, Leitner T. PrimerDesign-M: a multiple-alignment based multiple-primer design tool for walking across variable genomes. Bioinformatics 2015; 31:1472–1474 [CrossRef]
    [Google Scholar]
  51. Vilcek S, Herring AJ, Herring JA, Nettleton PF, Lowings JP et al. Pestiviruses isolated from pigs, cattle and sheep can be allocated into at least three genogroups using polymerase chain reaction and restriction endonuclease analysis. Arch Virol 1994; 136:309–323 [CrossRef]
    [Google Scholar]
  52. Kong HR, Anthony NB, Rowland KC, Khatri B, Kong BC. Genome re-sequencing to identify single nucleotide polymorphism markers for muscle color traits in broiler chickens. Asian-Australas J Anim Sci 2018; 31:13–18 [CrossRef]
    [Google Scholar]
  53. Moncla LH, Zhong G, Nelson CW, Dinis JM, Mutschler J et al. Selective bottlenecks shape evolutionary pathways taken during mammalian adaptation of a 1918-like avian influenza virus. Cell Host Microbe 2016; 19:169–180 [CrossRef]
    [Google Scholar]
  54. Varble A, Albrecht RA, Backes S, Crumiller M, Bouvier NM et al. Influenza A virus transmission bottlenecks are defined by infection route and recipient host. Cell Host Microbe 2014; 16:691–700 [CrossRef]
    [Google Scholar]
  55. Ridpath JF, Bayles DO, Neill JD, Falkenberg SM, Bauermann FV et al. Comparison of the breadth and complexity of bovine viral diarrhea (BVDV) populations circulating in 34 persistently infected cattle generated in one outbreak. Virology 2015; 485:297–304 [CrossRef]
    [Google Scholar]
  56. Dow N, Chernick A, Orsel K, van Marle G, van der Meer F. Genetic variability of bovine viral diarrhea virus and evidence for a possible genetic bottleneck during vertical transmission in persistently infected cattle. PLoS One 2015; 10:e0131972 [CrossRef]
    [Google Scholar]
  57. Chernick A, van der Meer F. Evolution of bovine viral diarrhea virus in Canada from 1997 to 2013. Virology 2017; 509:232–238 [CrossRef]
    [Google Scholar]
  58. Chernick A, Ambagala A, Orsel K, Wasmuth JD, van Marle G et al. Bovine viral diarrhea virus genomic variation within persistently infected cattle. Infect Genet Evol 2018; 58:218–223 [CrossRef]
    [Google Scholar]
  59. Tong SP, Li JS, Vitvitski L, Trépo C. Replication capacities of natural and artificial precore stop codon mutants of hepatitis B virus: relevance of pregenome encapsidation signal. Virology 1992; 191:237–245 [CrossRef]
    [Google Scholar]
  60. Cassini R, De Mitri MS, Gibellini D, Urbinati L, Bagaglio S et al. A novel stop codon mutation within the hepatitis B surface gene is detected in the liver but not in the peripheral blood mononuclear cells of HIV-infected individuals with occult HBV infection. J Viral Hepat 2013; 20:42–49 [CrossRef]
    [Google Scholar]
  61. Moratorio G, Henningsson R, Barbezange C, Carrau L, Bordería AV et al. Attenuation of RNA viruses by redirecting their evolution in sequence space. Nat Microbiol 2017; 2:17088 [CrossRef]
    [Google Scholar]
  62. Wang F-I, Deng M-C, Huang Y-L, Chang C-Y. Structures and functions of pestivirus glycoproteins: not simply surface matters. Viruses 2015; 7:3506–3529 [CrossRef]
    [Google Scholar]
  63. Gripshover EM, Givens MD, Ridpath JF, Brock KV, Whitley EM et al. Variation in E(rns) viral glycoprotein associated with failure of immunohistochemistry and commercial antigen capture ELISA to detect a field strain of bovine viral diarrhea virus. Vet Microbiol 2007; 125:11–21 [CrossRef]
    [Google Scholar]
  64. Sanjuán R, Codoñer FM, Moya A, Elena SF. Natural selection and the organ-specific differentiation of HIV-1 V3 hypervariable region. Evolution 2004; 58:1185–1194 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000343
Loading
/content/journal/mgen/10.1099/mgen.0.000343
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error