Genome constellations of rotavirus a isolated from avian species in Brazil, 2008–2015

A Correction to this article was published on 04 December 2020

This article has been updated

Abstract

Rotaviruses are members of the family Reoviridae and are a common cause of acute diarrhea in many mammalian and avian species. They are non-enveloped icosahedral particles and their genome comprises 11 segments of double-stranded RNA, which encodes six structural proteins (VP1–4, VP6–7) and six nonstructural proteins (NSP1–6). Genotypes are defined based upon the diversity found in these genes and viral characterization plays a central role on epidemiological studies and prevention. Here we investigate the distribution of Brazilian RVAs genotypes in 8 chicken samples collected between 2008 and 2015 from different regions by RT-PCR, partial (Sanger) nucleotide sequencing and phylogenetic analysis from all rotavirus genes. Although the identified genotypes were typical from avian host species, when analyzed together, they form novel genetic constellations: G19-P[31]-I11-R6-C6-M7-A16-N6-T8-E10-H8 and G19-P[31]-I4-R4-C4-M4-A16-N4-T4-E4-H4. This study highlights that avian rotaviruses are widespread among commercial farms in Brazil, and the co-circulation of at least two different genomic constellations indicates that may present a way bigger genetic variability, that can be increased by the possible transmission events from other birds, lack of specific preventive measures, as well as the different viral evolution mechanisms.

This is a preview of subscription content, access via your institution.

Fig. 1

Change history

  • 04 December 2020

    A Correction to this paper has been published: <ExternalRef><RefSource>https://doi.org/10.1007/s42770-020-00407-w</RefSource><RefTarget Address="10.1007/s42770-020-00407-w" TargetType="DOI"/></ExternalRef>

References

  1. 1.

    Desselberger U (2014) Rotaviruses. Virus Res 190:75–96. https://doi.org/10.1016/j.virusres.2014.06.016

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Luchs A, Timenetsky MC (2016) Group a rotavirus gastroenteritis: post-vaccine era, genotypes and zoonotic transmission. Einstein 14:278–287. https://doi.org/10.1590/S1679-45082016RB3582

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Sadiq A, Bostan N, Yinda KC, Naseem S, Sattar S (2018) Rotavirus: genetics, pathogenesis and vaccine advances. Rev Med Virol 28:e2003. https://doi.org/10.1002/rmv.2003

    Article  PubMed  Google Scholar 

  4. 4.

    Dhama K, Saminathan M, Karthik K, Tiwari R, Shabbir MZ, Kumar N, Malik YS, Singh RK (2015) Avian rotavirus enteritis - an updated review. Vet Q 35:142–158. https://doi.org/10.1080/01652176.2015.1046014

    Article  PubMed  Google Scholar 

  5. 5.

    ICVT 2018b International Committee for the Taxonomy of viruses. Taxonomy. Available at: https://talk.ictvonline.org/ . Accessed 25 Oct 2019

  6. 6.

    Estes MK, Greenberg HD (2013) Rotaviruses. In: Knipe DM, Howley PM (eds) Fields Virology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1347–1401

    Google Scholar 

  7. 7.

    Ogden KM, Snyder MJ, Dennis AF, Patton JT (2014) Predicted structure and domain organization of rotavirus capping enzyme and innate immune antagonist VP3. J Virol 88:9072–9085. https://doi.org/10.1128/JVI.00923-14

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Bányai K, Kemenesi G, Budinski I, Földes F, Zana B, Marton S, Varga-Kugler R, Oldal M, Kurucz K, Jakab F (2017) Candidate new rotavirus species in Schreiber's bats, Serbia. Infect Genet Evol 48:19–26. https://doi.org/10.1016/j.meegid.2016.12.002

    Article  PubMed  Google Scholar 

  9. 9.

    Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gómara M, Maes P, Patton JT, Rahman M, Van Ranst M (2008) Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82:3204–3219. https://doi.org/10.1128/JVI.02257-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Ito H, Sugiyama M, Masubuchi K, Mori Y, Minamoto N (2001) Complete nucleotide sequence of a group a avian rotavirus genome and a comparison with its counterparts of mammalian rotaviruses. Virus Res 75:123–138. https://doi.org/10.1016/s0168-1702(01)00234-9

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Trojnar E, Otto P, Johne R (2009) The first complete genome sequence of a chicken group a rotavirus indicates independent evolution of mammalian and avian strains. Virology 386:325–333. https://doi.org/10.1016/j.virol.2009.01.034

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Trojnar E, Sachsenröder J, Twardziok S, Reetz J, Otto PH, Johne R (2013) Identification of an avian group a rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol 94:136–142. https://doi.org/10.1099/vir.0.047381-0

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Beserra LAR, Barbosa BRP, Bernardes NTCG, Brandão PE, Gregori F (2014) Occurrence and characterization of rotavirus a in broilers, layers, and broiler breeders from Brazilian poultry farms. Avian Dis 58:153–157. https://doi.org/10.1637/10626-080513-ResNote.1

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Asano KM, Gregori F, Souza SP, Rotava D, Oliveira RN, Villarreal LY, Richtzenhain LJ, Brandão PE (2011) Bovine rotavirus in turkeys with enteritis. Avian Dis 55:697–701. https://doi.org/10.1637/9765-041911-ResNote.1

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Silva LC, Sanches AA, Gregori F, Brandão PE, Alfieri AA, Headley SA, Jerez JA (2012) First description of group a rotavirus from fecal samples of ostriches (Struthio camelus). Res Vet Sci 93:1066–1069. https://doi.org/10.1016/j.rvsc.2011.12.007

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404

    CAS  Article  Google Scholar 

  17. 17.

    Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  18. 18.

    Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    CAS  Article  Google Scholar 

  19. 19.

    Nei M, Kumar S (2000) Molecular evolution and Phylogenetics. Oxford University Press, New York

    Google Scholar 

  20. 20.

    Maes P, Matthijnssens J, Rahman M, Van Ranst M (2009) RotaC: a web-based tool for the complete genome classification of group a rotaviruses. BMC Microbiol 9:238. https://doi.org/10.1186/1471-2180-9-238

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Schumann T, Hotzel H, Otto P, Johne R (2009) Evidence of interspecies transmission and reassortment among avian group a rotaviruses. Virology 386:334–343. https://doi.org/10.1016/j.virol.2009.01.040

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Matthijnssens J, Rahman M, Ciarlet M, Zeller M, Heylen E, Nakagomi T, Uchida R, Hassan Z, Azim T, Nakagomi O, Van Ranst M (2010) Reassortment of human rotavirus gene segments into G11 rotavirus strains. Emerg Infect Dis 16:625–630. https://doi.org/10.3201/eid1604.091591

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Monini M, Zaccaria G, Ianiro G, Lavazza A, Vaccari G, Ruggeri FM (2014) Full-length genomic analysis of porcine rotavirus strains isolated from pigs with diarrhea in northern Italy. Infect Genet Evol 25:4–13. https://doi.org/10.1016/j.meegid.2014.03.024

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Nagai M, Shimada S, Fujii Y, Moriyama H, Oba M, Katayama Y, Tsuchiaka S, Okazaki S, Omatsu T, Furuya T, Koyama S, Shirai J, Katayama K, Mizutani T (2015) H2 genotypes of G4P[6], G5P[7], and G9[23] porcine rotaviruses show super-short RNA electropherotypes. Vet Microbiol 176:250–256. https://doi.org/10.1016/j.vetmic.2015.02.002

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Silva FDF, Espinoza LRL, Tonietti PO, Barbosa BR, Gregori F (2015) Whole-genomic analysis of 12 porcine group a rotaviruses isolated from symptomatic piglets in Brazil during the years of 2012-2013. Infect Genet Evol 32:239–254. https://doi.org/10.1016/j.meegid.2015.03.016

    Article  PubMed  Google Scholar 

  26. 26.

    Elschner M, Hotzel H, Reetz J, Diller R, Otto P (2005) Isolation, identification and characterization of group a rotavirus from a chicken: the inner capsid protein sequence shows only a distant phylogenetic relationship to most other avian group a rotaviruses. J Vet Med B Infect Dis Vet Public Health 52:211–213. https://doi.org/10.1111/j.1439-0450.2005.00848.x

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Silva RR, Bezerra DAM, Kaiano JHL, Manno MC, Oliveira DS, Sagica FES, Gabbay YB, Chaves SOC, Silva ALC, Alfieri AA, Mascarenhas JDP (2013) Molecular epidemiology of avian rotavirus in fecal samples of broiler chickens in Amazon region, Brazil, from august 2008 to may 2011. Rev Pan-Amaz Saúde 4:55–62. https://doi.org/10.5123/S2176-62232013000200007

    Article  Google Scholar 

  28. 28.

    Attoui H et al (2012) Family: Reoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: 9th report of the ICTV. Elsevier Academic Press, Amsterdam, pp 542–637

    Google Scholar 

Download references

Funding

This work was supported by the São Paulo Research Foundation (FAPESP)—Grant 2014/13531–7, Brazilian Government, by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code PROEX—Grant 1841/2016, and by Swedish Research Council—Project No. 2013–6772.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Laila A. R. Beserra.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Committee on Ethics for Animal Trials of the School of Veterinary Medicine, University of São Paulo, under protocol number 3070/2013.

Additional information

Publisher’s note

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

Responsible Editor: Giliane Souza Trindade

Electronic supplementary material

ESM 1

(DOCX 52 kb)

ESM 2

(DOCX 29 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Beserra, L.A.R., Barbosa, C.M., Berg, M. et al. Genome constellations of rotavirus a isolated from avian species in Brazil, 2008–2015. Braz J Microbiol 51, 1363–1375 (2020). https://doi.org/10.1007/s42770-020-00259-4

Download citation

Keywords

  • Rotavirus
  • Avian
  • Diversity
  • Genotypes
  • Sequence analysis
  • Phylogeny