Skip to main content
Log in

Genome-Wide Identification of Circular RNAs in Fungal Parasite Nosema ceranae

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Circular RNAs (circRNAs) are newly discovered endogenous non-coding RNAs (ncRNAs) that play key roles in microRNA function and transcriptional regulation. Though a large number of circRNAs had been identified in animals and plants, however, little is known regarding circRNAs in Nosema ceranae, a widespread fungal parasite of honeybee. In this study, using deep sequencing technology and bioinformatic analysis, we predicted 204 circRNAs from N. ceranae spore samples, including 174 exonic circRNAs and 30 intergenic circRNAs. In addition, the expression of seven N. ceranae circRNAs was confirmed by RT-PCR assay. Furthermore, regulation networks of circRNAs were constructed, and 15 circRNAs were found to act as sponges of the corresponding three miRNAs. GO categorization and pathway enrichment analysis suggested that the circRNAs are likely to play significant roles in N. ceranae spore. This is the first report of circRNAs generated by a microsporidia species. Our results provide novel insights into understanding the basic biology of N. ceranae.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221

    Article  CAS  Google Scholar 

  2. Andreeva K, Cooper NGF (2015) Circular RNAs: new players in gene regulation. Adv Biosci Biotechnol 6(6):433–441

    Article  CAS  Google Scholar 

  3. Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S (2014) CircRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56(1):55–66

    Article  CAS  Google Scholar 

  4. Botías C, Martín-Hernández R, Días J, García-Palencia P, Matabuena M, Juarranz A, Barrios L, Meana A, Nanetti A, Higes M (2012) The effect of induced queen replacement on Nosema, spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environ Microbiol 14(4):845–859

    Article  Google Scholar 

  5. Chen Y, Evans JD, Smith IB, Pettis JS (2008) Nosema ceranae, is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J Invertebr Pathol 97(2):186–188

    Article  Google Scholar 

  6. Cocquerelle C, Mascrez B, Hétuin D, Bailleul B (1993) Mis-splicing yields circular RNA molecules. Faseb J 7(1):155

    Article  CAS  Google Scholar 

  7. Cornman RS, Chen YP, Schatz MC, Street C, Zhao Y, Desany B, Egholm M, Hutchison S, Pettis JS, Lipkin WI, Evans JD (2009) Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 5(6):e1000466

    Article  Google Scholar 

  8. Ebert MS, Sharp PA (2010) Emerging roles for natural microRNA sponges. Current Biol 20(19):R858–R861

    Article  CAS  Google Scholar 

  9. Gao Y, Wang J, Zhao F (2015) CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol 16(1):4

    Article  CAS  Google Scholar 

  10. Guo JU, Agarwal V, Guo H, Bartel DP (2014) Expanded identification and characterization of mammalian circular RNAs. Genome Biol 15(7):409

    Article  Google Scholar 

  11. Hitoshi S, Zuo Y, Wang J, Zhang MQ, Malhotra A, Mayeda A (2006) Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res 34(8):e63

    Article  Google Scholar 

  12. Houseley JM, Garcia-Casado Z, Pascual M, Paricio N, O’Dell KM, Monckton DG, Artero RD (2006) Noncanonical RNAs from transcripts of the Drosophila muscleblind gene. J Hered 97(3):253–260

    Article  CAS  Google Scholar 

  13. Huang WF, Solter L, Aronstein K, Huang Z (2015) Infectivity and virulence of Nosema ceranae and Nosema apis in commercially available north American honey bees. J Invertebr Pathol 124:107–113

    Article  Google Scholar 

  14. Huang Q, Evans JD (2016) Identification of microRNA-like small RNAs from fungal parasite Nosema ceranae. J Invertebr Pathol 133:107–109

    Article  CAS  Google Scholar 

  15. Jayakodi M, Jung JW, Park D, Ahn YJ, Lee SC, Shin SY, Shin C, Yang TJ, Kwon HW (2015) Genome-wide characterization of long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera. BMC Genomics 16(1):680

    Article  Google Scholar 

  16. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19(2):141–157

    Article  CAS  Google Scholar 

  17. Kos A, Dijkema R, Arnberg AC, van der Meide PH, Schellekens H (1986) The hepatitis delta (|[delta]|) virus possesses a circular RNA. Nature 323(6088):558–560

    Article  CAS  Google Scholar 

  18. Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, Laneve P, Rajewsky N, Bozzoni I (2017) Circ-znf609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell 66(1):22–37

    Article  CAS  Google Scholar 

  19. Li F, Zhang L, Li W, Deng J, Zheng J, An M, Lu J, Zhou Y (2015) Circular RNA ITCH has inhibitory effect on ESCC by suppressing the Wnt/β-catenin pathway. Oncotarget 6(8):6001–6013

    PubMed  PubMed Central  Google Scholar 

  20. Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, Zhu P, Chang Z, Wu Q, Zhao Y, Jia Y, Xu P, Liu H, Shan G (2015) Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 22(3):256–264

    Article  CAS  Google Scholar 

  21. Liu J, Liu T, Wang X, He A (2017) Circles reshaping the RNA world: from waste to treasure. Mol Cancer 16(1):58

    Article  CAS  Google Scholar 

  22. Liang G, Yang Y, Niu G, Tang Z, Li K (2017) Genome-wide profiling of Sus scrofa circular RNAs across nine organs and three developmental stages. DNA Res 24(5):523–535

    Article  CAS  Google Scholar 

  23. Lu T, Cui L, Zhou Y, Zhu C, Fan D, Gong H, Zhao Q, Zhou C, Zhao Y, Lu D, Luo J, Wang Y, Tian Q, Feng Q, Huang T, Han B (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA 21(12): 2076–2087

  24. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338

    Article  CAS  Google Scholar 

  25. Odelius K, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27(3):431–432

    Article  Google Scholar 

  26. Pettis JS, vanEngelsdorp D, Johnson J, Dively G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99(2):153–158

    Article  CAS  Google Scholar 

  27. Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K, Li H (2015) Circular RNA: a new star of noncoding RNAs. Cancer Lett 365(2):141–148

    Article  CAS  Google Scholar 

  28. Rybak-Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, Herzog M, Schreyer L, Papavasileiou P, Ivanov A, Öhman M, Refojo D, Kadener S, Rajewsky N (2015) Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell 58(5):870–885

    Article  CAS  Google Scholar 

  29. Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK (1976) Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci USA 73(11):3852–3856

    Article  CAS  Google Scholar 

  30. St LG, Wahlestedt C, Kapranov P (2015) The landscape of long noncoding RNA classification. Trends Genet 31(5):239–251

    Article  Google Scholar 

  31. Tay Y, Rinn J, Pandolfi PP (2014) The multilayered complexity of ceRNA crosstalk and competition. Nature 505(7483):344–352

    Article  CAS  Google Scholar 

  32. Vivares CP, Gouy M, Thomarat F, Méténier G (2002) Functional and evolutionary analysis of a eukaryotic parasitic genome. Curr Opin Microbiol 5(5):499–505

    Article  CAS  Google Scholar 

  33. Xiao H, Yuan Z, Guo D, Hou B, Yin C, Zhang W, Li F (2015) Genome-wide identification of long noncoding RNA genes and their potential association with fecundity and virulence in rice brown planthopper, Nilaparvata lugens. BMC Genomics 16(1):1–16

    Article  Google Scholar 

  34. Zhang Y, Fan X, Mao M, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL (2013) Circular intronic long noncoding RNAs. Mol Cell 51(6):792–806

    Article  CAS  Google Scholar 

  35. Zuo J, Wang Q, Zhu B, Luo Y, Gao L (2016) Deciphering the roles of circRNAs on chilling injury in tomato. Biochem Bioph Res Commun 479(2):132–138

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank all editors and reviewers for their invaluable comments and recommendations that improved this work. This work was founded by the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-44-KXJ7), the Science and Technology Planning Project of Fujian Province (2018J05042), the Education and Scientific Research Fund of Young Teachers of Fujian Educational Bureau (JAT170158), the Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2017342,CXZX2017343), and the Open Fund of Key Laboratory of Pollinating Insect Biology of Ministry of Agriculture and Rural Affairs (2017MFNZS02).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dafu Chen.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, R., Chen, D., Chen, H. et al. Genome-Wide Identification of Circular RNAs in Fungal Parasite Nosema ceranae. Curr Microbiol 75, 1655–1660 (2018). https://doi.org/10.1007/s00284-018-1576-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-018-1576-z

Navigation