Skip to main content
SpringerLink
Log in

Eimeria tenella: a novel dsRNA virus in E. tenella and its complete genome sequence analysis

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Protozoa double-stranded (ds) RNA viruses have been described in Trichomonas, Giardia, and Leishmania. In this study, dsRNA and virus-like particles (approximately 30 nm in diameter) were discovered in Eimeria tenella sporulated oocysts. The complete genome of this novel dsRNA virus was sequenced using a three-step strategy. The sequencing results showed that the complete genome sequence was 6006 bp containing two open reading frames (ORFs) (2367 bp for ORF1 and 3216 bp for ORF2) with a five-nucleotide overlap (UGA/UG). The predicted ORF1 and ORF2 encoded a putative capsid protein of 788 amino acids (84.922 kDa) and a putative RNA-dependent RNA polymerase (RdRp) protein of 1071 amino acids (118.190 kDa). BLASTp analysis showed that the amino acid sequences for the E. tenella virus shared similarity with the E. brunetti RNA virus, with 29% homology in capsid proteins and 36% in RDRP proteins. The two untranslated regions were 349 bp (5′ UTR) and 78 bp (3′ UTR). The complete genome sequence of the E. tenella virus resembled characteristics of the Totiviridae family, indicating that this virus was a novel member of Totiviridae. Surprisingly, phylogenetic analysis showed that the E. tenella virus, E. brunetti RNA virus 1, and Mycoviruses were clustered into the genus Victorivirus and separated from the reported protozoa viruses, strongly suggesting a novel Eimeriaviruses subgenus. To the best of our knowledge, this is the first report for the complete genome sequence of the E. tenella virus. Using the nomenclature generally adopted for viruses, this new isolate was named E. tenella RNA virus 1. This study provides a foundation basis for further research on the biological characteristics of Eimeriaviruses.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. ICTV 2014 Master Species List (MSL)

  2. L.S. Diamond, C.F. Mattern, I.L. Bartgis, Viruses of Entamoeba histolytica. I. Identification of transmissible virus-like agents. J. Virol. 9, 326–341 (1972)

    CAS  PubMed  PubMed Central  Google Scholar 

  3. A.L. Wang, C.C. Wang, The double-stranded RNA in Trichomonas vaginalis may originate from virus-like particles. Proc. Natl. Acad. Sci. USA 83, 7956–7960 (1986)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. A.L. Wang, C.C. Wang, Discovery of a specific double-stranded RNA virus in Giardia lamblia. Mol. Biochem. Parasit. 21, 269–276 (1986)

    Article  CAS  Google Scholar 

  5. R.L. Miller, A.L. Wang, C.C. Wang, Purification and characterization of the Giardia lamblia double-stranded RNA virus. Mol. Biochem. Parasit. 28, 189–195 (1988)

    Article  CAS  Google Scholar 

  6. P.I. Tarr, R.F. Aline, B.L. Smiley, J. Scholler, J. Keithly, K. Stuart, LR1: a candidate RNA virus of Leishmania. Proc. Natl. Acad. Sci. USA 85, 9572–9575 (1988)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. K. Stuart, R. Week, C. Tripp, B. Smiley, J.R. Aline, Virus and Episomes of Leishmania Immune Recognition and Evasion: Molecular Aspects of Host Parasite Interaction (Academic Press, London, 1990), pp. 269–278

    Book  Google Scholar 

  8. H. Revets, D. Dekegel, W. Deleersnijder, J. Jonckheere, J. Peeters, E. Leysen, R. Hamers, Identification of virus-like particles in Eimeria stiedae. Mol. Biochem. Parasit. 36, 209–215 (1989)

    Article  CAS  Google Scholar 

  9. T. Sepp, R. Entzeroth, J. Mertsching, P.H. Hofschneider, R. Kandolf, Novel ribonucleic acid species in Eimeria nieschulzi are associated with RNA-dependent RNA polymerase activity. Parasitol. Res. 77, 581–584 (1991)

    Article  CAS  PubMed  Google Scholar 

  10. I. Roditi, T. Wyler, N. Smith, R. Braun, Virus-like particles in Eimeria nieschulzi are associated with multiple RNA segments. Mol. Biochem. Parasit. 63, 275–282 (1994)

    Article  CAS  Google Scholar 

  11. J. Ellis, H. Revets, Eimeria species which infect the chicken contain virus-like RNA molecules. Parasitology 101, 163–169 (1990)

    Article  CAS  PubMed  Google Scholar 

  12. Q. Han, J. Li, P. Gong, J. Gai, S. Li, X. Zhang, Virus-like particles in Eimeria tenella are associated with multiple RNA segments. Exp. Parasitol. 127, 646–650 (2011)

    Article  CAS  PubMed  Google Scholar 

  13. S. Lee, M.A. Fernando, E. Nagy, dsRNA associated with virus-like particles in Eimeria spp. of the domestic fowl. Parasitol. Res. 82, 518–523 (1996)

    Article  CAS  PubMed  Google Scholar 

  14. N.V. Khramtsov, K.M. Woods, M.V. Nesterenko, C.C. Dykstra, S.J. Upton, Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Mol. Microbiol. 26, 289–300 (1997)

    Article  CAS  PubMed  Google Scholar 

  15. R.B. Williams, Epidemiological aspects of the use of live anticoccidial vaccines for chickens. Int. J. Parasitol. 28, 1089–1098 (1998)

    Article  CAS  PubMed  Google Scholar 

  16. P. Scott, Leishmania-a parasitized parasite. New. Engl. J. Med. 364, 1773–1774 (2011)

    Article  CAS  PubMed  Google Scholar 

  17. A. Ives, C. Ronet, F. Prevel, G. Ruzzante, S. Fuertes-Marraco, F. Schutz, H. Zangger, M. Revaz-Breton, L.F. Lye, S.M. Hickerson, S.M. Beverley, H. Acha-Orbea, P. Launois, N. Fasel, S. Masina, Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331, 775–778 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. H. Attoui, F. Billoir, J.F. Cantaloube, P. Biagini, P. Micco, X. Lamballerie, Strategies for the sequence determination of viral dsRNA genomes. J. Virol. Methods 89, 147–158 (2000)

    Article  CAS  PubMed  Google Scholar 

  19. S. Maan, S. Rao, N.S. Maan, S.J. Anthony, H. Attoui, A.R. Samuel, P.P. Mertens, Rapid cDNA synthesis and sequencing techniques for the genetic study of bluetongue and other dsRNA viruses. J. Virol. Methods 143, 132–139 (2007)

    Article  CAS  PubMed  Google Scholar 

  20. A.C. Potgieter, N.A. Page, J. Liebenberg, I.M. Wright, O. Landt, A.A. van Dijk, Improved strategies for sequence-independent amplification and sequencing of viral double-stranded RNA genomes. J. Gen. Virol. 90, 1423–1432 (2009)

    Article  CAS  PubMed  Google Scholar 

  21. F.T. Vreede, M. Cloete, G.B. Napier, A.A. Dijk, G.J. Viljoen, Sequence-independent amplification and cloning of large dsRNA virus genome segments by poly(dA)-oligonucleotide ligation. J. Virol. Methods 72, 243–247 (1998)

    Article  CAS  PubMed  Google Scholar 

  22. M.W. Shirley, A.C. Bushell, J.E. Bushell, V. McDonald, B. Roberts, A live attenuated vaccine for the control of avian coccidiosis: trials in broiler breeders and replacement layer flocks in the United Kingdom. Vet. Rec. 137, 453–457 (1995)

    Article  CAS  PubMed  Google Scholar 

  23. A.E. Bashar, J. Cai, M. Xie, G. Li, Z. Qin, H. Wu, X. Peng, W. Wei, Characterization of microneme-2 (EtMIC-2) gene of Eimeria tenella Guangdong strain. Int. J. Poultry. Sci. 113, 133–138 (2003)

    Google Scholar 

  24. Anita Haug, R.B. Williams, S. Larsen, Counting coccidial oocysts in chicken faeces: a comparative study of a standard McMaster technique and a new rapid method[J]. Vet. Parasitol. 13, 233–242 (2006)

    Article  Google Scholar 

  25. J.L. Dale, D.A. Phillips, J.N. Parry, Double-stranded RNA in Banana plants with bunchy top disease[J]. J. Gen. Virol. 67(2), 371–375 (1986)

    Article  CAS  Google Scholar 

  26. J.A. Dodds, M. Bar-Joseph, Double-stranded RNA from plants infected with closteroviruses. Phytopathology. 73, 419–423 (1983)

    Article  CAS  Google Scholar 

  27. P.L. Hunst, F.M. Latterell, A.E. Rossi, Variation in double stranded RNA from isolates of Pyricularia oryzae. Phytopathology. 76, 674–678 (1986)

    Article  CAS  Google Scholar 

  28. V.K. Singh, A.K. Mangalam, S. Dwivedi, S. Naik, Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24, 318–319 (1998)

    CAS  PubMed  Google Scholar 

  29. H. Telenius, N.P. Carter, C.E. Bebb, M. Nordenskjo, B.A. Ponder, A. Tunnacliffe, Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics 13, 718–725 (1992)

    Article  CAS  PubMed  Google Scholar 

  30. D.J. Korbie, J.S. Mattick, Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat. Protoc. 3, 1452–1456 (2008)

    Article  CAS  PubMed  Google Scholar 

  31. D.S. Prestridge, Predicting Pol II promoter sequences using transcription factor binding sites. J. Mol. Biol. 249, 923–932 (1995)

    Article  CAS  PubMed  Google Scholar 

  32. J.D. Thompson, D.G. Higgins, T.J. Gibson, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. F. Felsenstein, PHYLIP (phylogeny inference package) version 3.67. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA (2007)

  34. A. Rambaut, FigTree: Tree figure drawing tool, version 1.0. Institute of Evolutionary Biology, University of Edinburgh (2006). http://tree.bio.ed.ac.uk/software/figtree/

  35. S.A. Ghabrial, M.L. Nibert, Victorivirus, a new genus of fungal viruses in the family Totiviridae[J]. Arch. Virol. 154(2), 373–379 (2009)

    Article  CAS  PubMed  Google Scholar 

  36. P. Mertens, The dsRNA viruses. Virus Res. 101, 3–13 (2004)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Nos. 31072123, 31272550, and 31372425), Program for New Century Excellent Talents in University.

Author information

Author notes

    Authors and Affiliations

    1. College of Veterinary Medicine, Jilin University, 5333 Xi’an Road, Changchun, 130062, China

      Bin Wu, Xichen Zhang, Pengtao Gong, Mingying Li, He Ding, Caiyan Xin, Na Zhao & Jianhua Li

    Authors
    1. Bin Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Xichen Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Pengtao Gong
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Mingying Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. He Ding
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Caiyan Xin
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Na Zhao
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Jianhua Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Jianhua Li.

    Additional information

    Edited by A. Lorena Passarelli.

    Bin Wu, Xichen Zhang, and Pengtao Gong have contributed equally to this study.

    Electronic supplementary material

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Wu, B., Zhang, X., Gong, P. et al. Eimeria tenella: a novel dsRNA virus in E. tenella and its complete genome sequence analysis. Virus Genes 52, 244–252 (2016). https://doi.org/10.1007/s11262-016-1295-0

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11262-016-1295-0

    Keywords

    Search

    Navigation