Skip to main content

Advertisement

SpringerLink
Log in

Columbid circoviruses detected in free ranging pigeons from Southern Brazil: insights on PiCV evolution

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

A Correction to this article was published on 24 August 2018

This article has been updated

Abstract

Pigeon circovirus (PiCV) is taxonomically classified as a member of the Circovirus genus, family Circoviridae. The virus contains a single stranded DNA genome of approximately 2 kb, with minor length variations among different isolates. The occurrence of PiCV infections in pigeons (Columba livia) has been documented worldwide over the past 20 years; however, in Brazil there were still no reports on PiCV detection. This study identifies seven PiCV genomes recovered from domestic pigeons of South Brazil through high-throughput sequencing and shows a high frequency of PiCV infection, through quantitative real-time PCR. Phylogenetic classification was performed by maximum likelihood analysis of the full genomes, ORF V1 (Rep) and ORF C1 (Cap). The results show that either full genome or Cap based analysis allowed PiCV classification into five major clades (groups A to E), where Brazilian sequences were classified as A, C or D. Recombination analyses were carried out with Simplot and RDP4 and the results show that both Rep and Cap ORFs contain several recombination hotspots, pointing to an important role for such events in PiCV 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

Change history

  • 24 August 2018

    Unfortunately, the word “evolution” was found missing in title of the original article which is corrected here by this erratum. The original article has been corrected.

References

  1. Mankertz A, Hattermann K, Ehlers B, Soike D (2000) Cloning and sequencing of columbid circovirus (CoCV), a new circovirus from pigeons. Arch Virol 145:2469–2479. https://doi.org/10.1007/s007050070002

    Article  CAS  PubMed  Google Scholar 

  2. Duchatel JP, Todd D, Curry A et al (2005) New data on the transmission of pigeon circovirus. Vet Rec 157:413–415. https://doi.org/10.1136/vr.157.14.413

    Article  CAS  PubMed  Google Scholar 

  3. Rosario K, Breitbart M, Harrach B et al (2017) Revisiting the taxonomy of the family Circoviridae: establishment of the genus Cyclovirus and removal of the genus Gyrovirus. Arch Virol 162:1447–1463. https://doi.org/10.1007/s00705-017-3247-y

    Article  CAS  PubMed  Google Scholar 

  4. Stenzel T, Farkas K, Varsani A (2015) Genome sequence of a diverse goose circovirus recovered from greylag goose. Genome Announc. https://doi.org/10.1128/genomeA.00767-15

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cságola A, Lőrincz M, Tombácz K et al (2012) Genetic diversity of pigeon circovirus in Hungary. Virus Genes 44:75–79. https://doi.org/10.1007/s11262-011-0669-6

    Article  CAS  PubMed  Google Scholar 

  6. Yamamoto E, Ito H, Kitamoto E et al (2015) Complete genome sequence of pigeon circovirus detected in racing pigeons in western Japan. Virus Genes 51:140–143. https://doi.org/10.1007/s11262-015-1211-z

    Article  CAS  PubMed  Google Scholar 

  7. Delwart E, Li L (2012) Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes. Virus Res 164:114–121. https://doi.org/10.1016/j.virusres.2011.11.021

    Article  CAS  PubMed  Google Scholar 

  8. Todd D, Weston JH, Soike D, Smyth JA (2001) Genome sequence determinations and analyses of novel circoviruses from goose and pigeon. Virology 286:354–362. https://doi.org/10.1006/viro.2001.0985

    Article  CAS  PubMed  Google Scholar 

  9. Woods LW, Latimer KS, Niagro FD et al (1994) A retrospective study of circovirus infection in pigeons: nine cases (1986–1993). J Vet Diagn Invest 6:156–164. https://doi.org/10.1177/104063879400600205

    Article  CAS  PubMed  Google Scholar 

  10. Julian L, Piasecki T, Chrzastek K et al (2013) Extensive recombination detected among beak and feather disease virus isolates from breeding facilities in Poland. J Gen Virol 94:1086–1095. https://doi.org/10.1099/vir.0.050179-0

    Article  CAS  PubMed  Google Scholar 

  11. Ng TFF, Willner DL, Lim YW et al (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE. https://doi.org/10.1371/journal.pone.0020579

    Article  PubMed  PubMed Central  Google Scholar 

  12. Dean FB (2001) Rapid amplification of plasmid and phage DNA using Phi29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 11:1095–1099. https://doi.org/10.1101/gr.180501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lasken RS (2009) Genomic DNA amplification by the multiple displacement amplification (MDA) method: figure 1. Biochem Soc Trans 37:450–453. https://doi.org/10.1042/BST0370450

    Article  CAS  PubMed  Google Scholar 

  14. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Schmidt HA, Petzold E, Vingron M, von Haeseler A (2003) Molecular phylogenetics: parallelized parameter estimation and quartet puzzling. J Parallel Distrib Comput 63:719–727. https://doi.org/10.1016/S0743-7315(03)00129-1

    Article  Google Scholar 

  16. Guindon S, Dufayard J-F, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  17. Lefort V, Longueville J-E, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34:2422–2424. https://doi.org/10.1093/molbev/msx149

    Article  PubMed  PubMed Central  Google Scholar 

  18. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552. https://doi.org/10.1080/10635150600755453

    Article  PubMed  Google Scholar 

  19. Rambaut A (2009) FigTree v1.4: tree figure drawing tool [Internet]

  20. Yu G, Smith DK, Zhu H et al (2017) GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36. https://doi.org/10.1111/2041-210X.12628

    Article  Google Scholar 

  21. Muhire B, Martin DP, Brown JK et al (2013) A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). Arch Virol 158:1411–1424. https://doi.org/10.1007/s00705-012-1601-7

    Article  CAS  PubMed  Google Scholar 

  22. Lole KS, Bollinger RC, Paranjape RS et al (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Sambrook J, Russel DW (2001) Molecular cloning—a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  24. Stenzel T, Piasecki T, Chrzstek K et al (2014) Pigeon circoviruses display patterns of recombination, genomic secondary structure and selection similar to those of beak and feather disease viruses. J Gen Virol 95:1338–1351. https://doi.org/10.1099/vir.0.063917-0

    Article  CAS  PubMed  Google Scholar 

  25. Bencke GA (2007) POMBOS-DOMÉSTICOS Sugestões para o controle em escolas públicas estaduais. http://www.FzbRsGovBr/Upload/20150514114242Pombos_DomesticosPdf. 23

  26. Fontoura PM, Dyer E, Blackburn TM, Orsi ML (2013) Non-native bird species in Brazil Espécies. Neotrop Biol Conserv 8:165–175. https://doi.org/10.4013/nbc.2013.83.07

    Article  Google Scholar 

  27. Duchatel JP, Todd D, Smyth JA et al (2006) Observations on detection, excretion and transmission of pigeon circovirus in adult, young and embryonic pigeons. Avian Pathol 35:30–34. https://doi.org/10.1080/03079450500465692

    Article  CAS  PubMed  Google Scholar 

  28. Stenzel TA, Pestka D, Tykałowski B et al (2012) Epidemiological investigation of selected pigeon viral infections in Poland. Vet Rec 171:562. https://doi.org/10.1136/vr.100932

    Article  CAS  PubMed  Google Scholar 

  29. Wang K-C, Zhuang Q, Qiu Y et al (2017) Genome sequence characterization of pigeon circoviruses in China. Virus Res 233:1–7. https://doi.org/10.1016/j.virusres.2017.03.007

    Article  CAS  PubMed  Google Scholar 

  30. Lefeuvre P, Lett J-M, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707. https://doi.org/10.1128/JVI.02152-08

    Article  CAS  PubMed  Google Scholar 

  31. Varsani A, de Villiers GK, Regnard GL et al (2010) A unique isolate of beak and feather disease virus isolated from budgerigars (Melopsittacus undulatus) in South Africa. Arch Virol 155:435–439. https://doi.org/10.1007/s00705-010-0589-0

    Article  CAS  PubMed  Google Scholar 

  32. Lemey P, Posada D (2009) Introduction to recombination detection. In: Lemey P, Salemi M, Vandamme A-M (eds) The phylogenetic handbook, 2nd edn. Cambridge University Press, Cambridge, pp 493–517

    Chapter  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Mr. Luis Gustavo Trainini, who kindly gave access to the samples. This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Financiadora de Estudos e Projetos (FINEP, contract 01.10.0783.00). P.M.R. has a CNPq 1A research fellow. This work was carried out as part of the doctoral studies of M.R.L (Programa de Pós-graduação em Ciências Veterinárias, UFRGS).

Author information

Authors and Affiliations

  1. Laboratório de Virologia, Departamento de Microbiologia, Imunologia e Parasitologia, Instituto de Ciências Básicas da Saúde, UFRGS, Av. Sarmento Leite 500, sala 208, Porto Alegre, Rio Grande do Sul, CEP 90050-170, Brazil

    M. R. Loiko, A. P. M. Varela, C. Tochetto, C. M. Scheffer, D. A. Lima, C. Cerva, W. P. Paim & P. M. Roehe

  2. Laboratório de Biologia Molecular, Instituto de Pesquisas Veterinárias Desidério Finamor (IPVDF), Secretaria Estadual de Agricultura, Pecuária e Irrigação, Estrada Municipal do Conde, 6000, Eldorado do Sul, Rio Grande do Sul, CEP 92990-000, Brazil

    M. R. Loiko, A. P. M. Varela, C. Tochetto, D. A. Lima, C. Cerva, W. P. Paim & Fabiana Quoos Mayer

  3. Centro Universitário Ritter dos Reis-UniRitter, Laureate International Universities, Porto Alegre, Rio Grande do Sul, Brazil

    D. M. Junqueira

  4. Falcoaria e Consultoria Ambiental-HAYABUSA, São Francisco de Paula, RS, Brazil

    A. P. Morel

Authors
  1. M. R. Loiko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. M. Junqueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. P. M. Varela
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Tochetto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. M. Scheffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. A. Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. P. Morel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. C. Cerva
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. W. P. Paim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fabiana Quoos Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. P. M. Roehe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabiana Quoos Mayer.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Handling Editor: Sheela Ramamoorthy.

The original version of this article was revised: The word “evolution” was found missing in title of the original article and is corrected here.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 67 kb)

Fig.S1.

Place of origin of the free-living pigeons used in this study. The points marked on the map are the cities where the pigeons were captured. (DOCX 201 kb)

Fig.S2.

Likelihood mapping of five datasets comprising 82 PiCV sequences. A) Complete genome nucleotide sequences, B) Cap nucleotide sequences, C) Cap amino acid sequences, D) Rep nucleotide sequences, and E) Rep amino acid sequences. (DOCX 395 kb)

Fig. S3.

Bootscanning plots of six PiCV recombinant sequences. Bootscan analyses were performed on a sliding window of 200 nt by increments of 20 nt. A) Genotype A sequence showing no recombination profile; B) Genotype A (Table S1) sequence showing a recombination pattern around positions 1619-1826; C) Genotype A, break point positions around 1480-1826; D) Genotype C sequence presenting no recombination profile; E) and F) Recombination profiles of the sequences from Brazil in this study (genotype C*). (DOCX 818 kb)

Fig.S4.

Box plot of PiCV viral genome loads and the city of origin of sampled pigeons. (DOCX 136 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Loiko, M.R., Junqueira, D.M., Varela, A.P.M. et al. Columbid circoviruses detected in free ranging pigeons from Southern Brazil: insights on PiCV evolution. Arch Virol 163, 3083–3090 (2018). https://doi.org/10.1007/s00705-018-3990-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-018-3990-8

Search

Navigation