Skip to main content
SpringerLink
Log in

A new (old) bovine viral diarrhea virus 2 subtype: BVDV-2e

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Bovine pestiviruses are members of the species Pestivirus A (bovine viral diarrhea virus 1, BVDV-1), Pestivirus B (BVDV-2) or Pestivirus H (HoBiPeV). To date, BVDV-2 isolates/strains have been classified into three subtypes (a-c) by phylogenetic analysis, and an additional subtype (d) has been proposed based on 5' untranslated region (UTR) secondary structures. In a previous study, we identified some BVDV-2 sequences in the GenBank database that could not be classified as subtype a, b or c by phylogenetic analysis of their genomes, UTRs or individual genes. Here, we performed a detailed study of these sequences and assessed whether they might represent a distinct BVDV-2 subtype. Initially, we collected 85 BVDV-2 complete/near-complete genomes (CNCGs) from GenBank and performed a “proof of equivalence” between phylogenetic analyses based on CNCGs and open reading frames (ORFs), which showed that ORFs may be reliably used as a reference target for BVDV-2 phylogeny, allowing us to increase our dataset to 139 sequences. Among these, we found seven sequences that could not be classified as BVDV-2a-c. The same was observed in the phylogenetic analysis of CNCGs and viral genes. In addition, the seven non-BVDV-2a-c sequences formed a distinct cluster in all phylogenetic trees, which we propose to term BVDV-2e. BVDV-2e also showed 44 amino acid changes compared to BVDV-2a-c, 20 of which are in well-defined positions. Importantly, an additional phylogenetic analysis including BVDV-2d and a pairwise comparison of BVDV-2e and BVDV-2d sequences also supported the difference between these subtypes. Finally, we propose the recognition of BVDV-2e as a distinct BVDV-2 subtype and encourage its inclusion in future phylogenetic analyses to understand its distribution and evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and material

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Collett MS, Larson R, Belzer SK, Retzel E (1988) Proteins encoded by bovine viral diarrhea virus: the genomic organization of a pestivirus. Virology 165:200–208. https://doi.org/10.1016/0042-6822(88)90673-3

    Article  CAS  Google Scholar 

  2. Tautz N, Tews BA, Meyers G (2015) The molecular biology of pestiviruses. Adv Virus Res 93:47–160. https://doi.org/10.1016/bs.aivir.2015.03.002

    Article  CAS  Google Scholar 

  3. Yeşilbağ K, Alpay G, Becher P (2017) Variability and global distribution of subgenotypes of bovine viral diarrhea virus. Viruses 9:128. https://doi.org/10.3390/v9060128

    Article  CAS  Google Scholar 

  4. ICTV (2020) Genus: pestivirus—flaviviridae—positive-sense RNA viruses—ICTV. https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/flaviviridae/361/genus-pestivirus. Accessed 29 Jan 2021

  5. Becher P, Orlich M, Kosmidou A et al (1999) Genetic diversity of pestiviruses: identification of novel groups and implications for classification. Virology 262:64–71. https://doi.org/10.1006/viro.1999.9872

    Article  CAS  Google Scholar 

  6. de Oliveira FP, de Oliveira DB, Figueiredo LB et al (2019) Molecular detection and phylogeny of bovine viral diarrhea virus 1 among cattle herds from Northeast, Southeast, and Midwest regions, Brazil. Braz J Microbiol 50:571–577. https://doi.org/10.1007/s42770-019-00064-8

    Article  CAS  Google Scholar 

  7. Nagai M, Hayashi M, Sugita S et al (2004) Phylogenetic analysis of bovine viral diarrhea viruses using five different genetic regions. Virus Res 99:103–113. https://doi.org/10.1016/j.virusres.2003.10.006

    Article  CAS  Google Scholar 

  8. Ridpath JF, Bolin SR, Dubovi EJ (1994) Segregation of bovine viral diarrhea virus into genotypes. Virology 205:66–74. https://doi.org/10.1006/viro.1994.1620

    Article  CAS  Google Scholar 

  9. Vilček S, Herring AJ, Herring JA et al (1994) 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 136:309–323. https://doi.org/10.1007/BF01321060

    Article  Google Scholar 

  10. De Oliveira FC, De Oliveira PBS et al (2021) Sequence analysis of the DA domain of glycoprotein E2 of pestiviruses isolated from beef cattle in Southern Brazil. Arch Virol 1:3. https://doi.org/10.1007/s00705-020-04910-1

    Article  CAS  Google Scholar 

  11. Houe H (1999) Epidemiological features and economical importance of bovine virus diarrhoea virus (BVDV) infections. Vet Microbiol 64:89–107. https://doi.org/10.1016/S0378-1135(98)00262-4

    Article  CAS  Google Scholar 

  12. Pinior B, Firth CL, Richter V et al (2017) A systematic review of financial and economic assessments of bovine viral diarrhea virus (BVDV) prevention and mitigation activities worldwide. Prev Vet Med 137:77–92. https://doi.org/10.1016/J.PREVETMED.2016.12.014

    Article  Google Scholar 

  13. Gethmann J, Probst C, Bassett J et al (2019) An epidemiological and economic simulation model to evaluate strategies for the control of bovine virus diarrhea in Germany. Front Vet Sci. https://doi.org/10.3389/FVETS.2019.00406

    Article  Google Scholar 

  14. Pellerin C, Van Den Hurk J, Lecomte J, Tijssen P (1994) Identification of a new group of bovine viral diarrhea virus strains associated with severe outbreaks and high mortalities. Virology 203:260–268. https://doi.org/10.1006/viro.1994.1483

    Article  CAS  Google Scholar 

  15. Flores EF, Ridpath JF, Weiblen R et al (2002) Phylogenetic analysis of Brazilian bovine viral diarrhea virus type 2 (BVDV-2) isolates: evidence for a subgenotype within BVDV-2. Virus Res 87:51–60. https://doi.org/10.1016/S0168-1702(02)00080-1

    Article  CAS  Google Scholar 

  16. Tajima M, Frey H-R, Yamato O et al (2001) Prevalence of genotypes 1 and 2 of bovine viral diarrhea virus in Lower Saxony, Germany. Virus Res 76:31–42. https://doi.org/10.1016/S0168-1702(01)00244-1

    Article  CAS  Google Scholar 

  17. Jones LR, Zandomeni R, Weber EL (2001) Genetic typing of bovine viral diarrhea virus isolates from Argentina. Vet Microbiol 81:367–375. https://doi.org/10.1016/S0378-1135(01)00367-4

    Article  CAS  Google Scholar 

  18. Giangaspero M, Harasawa R, Weber L, Belloli A (2008) Genoepidemiological evaluation of bovine viral diarrhea virus 2 species based on secondary structures in the 5’ untranslated region. J Vet Med Sci 70:571–580. https://doi.org/10.1292/jvms.70.571

    Article  CAS  Google Scholar 

  19. de Oliveira PSB, Silva Júnior JVJ, Weiblen R, Flores EF (2021) Subtyping bovine viral diarrhea virus (BVDV): which viral gene to choose? Infect Genet Evol 92:104891. https://doi.org/10.1016/j.meegid.2021.104891

    Article  CAS  Google Scholar 

  20. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792. https://doi.org/10.1093/NAR/GKH340

    Article  CAS  Google Scholar 

  21. Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  Google Scholar 

  22. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083

    Article  CAS  Google Scholar 

  23. Owen M, Provan JS (2011) A fast algorithm for computing geodesic distances in tree space. IEEE/ACM Trans Comput Biol Bioinform 8:2–13. https://doi.org/10.1109/TCBB.2010.3

    Article  Google Scholar 

  24. Goluch T, Bogdanowicz D, Giaro K (2020) Visual TreeCmp: comprehensive comparison of phylogenetic trees on the web. Methods Ecol Evol 11:494–499. https://doi.org/10.1111/2041-210X.13358

    Article  Google Scholar 

  25. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277. https://doi.org/10.1371/journal.pone.0108277

    Article  CAS  Google Scholar 

  26. Tajima M (2004) Bovine viral diarrhea virus 1 is classified into different subgenotypes depending on the analyzed region within the viral genome. Vet Microbiol 99:131–138. https://doi.org/10.1016/j.vetmic.2003.11.011

    Article  CAS  Google Scholar 

  27. Workman AM, Heaton MP, Harhay GP et al (2016) Resolving Bovine viral diarrhea virus subtypes from persistently infected U.S. beef calves with complete genome sequence. J Vet Diagn Investig 28:519–528. https://doi.org/10.1177/1040638716654943

    Article  CAS  Google Scholar 

  28. Neill JD, Workman AM, Hesse R et al (2019) Identification of BVDV2b and 2c subgenotypes in the United States: genetic and antigenic characterization. Virology 528:19–29. https://doi.org/10.1016/j.virol.2018.12.002

    Article  CAS  Google Scholar 

  29. Weber MN, Streck AF, Silveira S et al (2015) Homologous recombination in pestiviruses: identification of three putative novel events between different subtypes/genogroups. Infect Genet Evol 30:219–224. https://doi.org/10.1016/j.meegid.2014.12.032

    Article  CAS  Google Scholar 

  30. Donis RO, Corapi W, Dubovi EJ (1988) Neutralizing monoclonal antibodies to bovine viral diarrhoea virus bind to the 56K to 58K glycoprotein. J Gen Virol 69(Pt 1):77–86. https://doi.org/10.1099/0022-1317-69-1-77

    Article  CAS  Google Scholar 

  31. Bolin S, Moennig V, Kelso Gourley NE, Ridpath J (1988) Monoclonal antibodies with neutralizing activity segregate isolates of bovine viral diarrhea virus into groups. Brief report. Arch Virol 99:117–123. https://doi.org/10.1007/BF01311029

    Article  CAS  Google Scholar 

  32. Lindenbach BD, Murray CL, Thiel HJ, Rice CM (2013) Flaviviridae. In: Fields virology. Lippincott Williams & Wilkins, Philadelphia, pp 712–746

  33. Bolin SR (1993) Immunogens of bovine viral diarrhea virus. Vet Microbiol 37:263–271. https://doi.org/10.1016/0378-1135(93)90028-6

    Article  CAS  Google Scholar 

  34. El Omari K, Iourin O, Harlos K et al (2013) Structure of a pestivirus envelope glycoprotein E2 clarifies its role in cell entry. Cell Rep 3:30–35. https://doi.org/10.1016/j.celrep.2012.12.001

    Article  CAS  Google Scholar 

  35. Tellinghuisen TL, Paulson MS, Rice CM (2006) The NS5A protein of bovine viral diarrhea virus contains an essential zinc-binding site similar to that of the hepatitis C virus NS5A protein. J Virol 80:7450. https://doi.org/10.1128/JVI.00358-06

    Article  CAS  Google Scholar 

Download references

Acknowledgments

PSBO is a graduate student of the Programa de Pós-graduação em Medicina Veterinária, UFSM, and thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Brazil) for his scholarship. EFF (process 301414/2010-6) and RW (process 304153/2014-1) were supported by CNPq research fellowships. The research was financed in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil—Finance code 001.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance code 001.

Author information

Authors and Affiliations

  1. Setor de Virologia, Departamento de Medicina Veterinária Preventiva, Universidade Federal de Santa Maria, Av. Roraima, 1000, Prédio 63A, Camobi, Santa Maria, Rio Grande do Sul, 97105-900, Brazil

    Pablo Sebastian Britto de Oliveira, José Valter Joaquim Silva Júnior, Rudi Weiblen & Eduardo Furtado Flores

  2. Programa de Pós-graduação em Medicina Veterinária, Universidade Federal de Santa Maria, Santa Maria, Rio Grande do Sul, Brazil

    Pablo Sebastian Britto de Oliveira

  3. Setor de Virologia, Laboratório de Imunopatologia Keizo Asami, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil

    José Valter Joaquim Silva Júnior

Authors
  1. Pablo Sebastian Britto de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Valter Joaquim Silva Júnior
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rudi Weiblen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eduardo Furtado Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PBSO performed the amino acid and phylogeny analyses and assisted in the experimental design, interpretation of results and manuscript preparation; JVJr assisted in the analysis of amino acids and phylogeny, experimental design, and interpretation of results and prepared the final version of the manuscript; RW assisted in the interpretation of results and manuscript review; and EFF assisted in the experimental design, interpretation of results, and elaboration and final review of the manuscript and guided the study.

Corresponding authors

Correspondence to José Valter Joaquim Silva Júnior or Eduardo Furtado Flores.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

Not applicable. This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Zhenhai Chen.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

705_2022_5565_MOESM1_ESM.doc

Supplementary File S1 Accession numbers of the BVDV-2 complete/near-complete genome sequences collected in our study (DOC 56 kb)

Supplementary File S2 Accession numbers of the BVDV-2 open reading frame sequences collected in our study (DOC 43 kb)

Supplementary File S3 Phylogenetic trees of BVDV-2 (uncompressed version) (PDF 2763 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Oliveira, P.S.B., Silva Júnior, J.V.J., Weiblen, R. et al. A new (old) bovine viral diarrhea virus 2 subtype: BVDV-2e. Arch Virol 167, 2545–2553 (2022). https://doi.org/10.1007/s00705-022-05565-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05565-w

Search

Navigation