Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Insect symbiotic bacteria harbour viral pathogens for transovarial transmission

Abstract

Many insects, including mosquitoes, planthoppers, aphids and leafhoppers, are the hosts of bacterial symbionts and the vectors for transmitting viral pathogens13. In general, symbiotic bacteria can indirectly affect viral transmission by enhancing immunity and resistance to viruses in insects35. Whether symbiotic bacteria can directly interact with the virus and mediate its transmission has been unknown. Here, we show that an insect symbiotic bacterium directly harbours a viral pathogen and mediates its transovarial transmission to offspring. We observe rice dwarf virus (a plant reovirus) binding to the envelopes of the bacterium Sulcia, a common obligate symbiont of leafhoppers68, allowing the virus to exploit the ancient oocyte entry path of Sulcia in rice leafhopper vectors. Such virus–bacterium binding is mediated by the specific interaction of the viral capsid protein and the Sulcia outer membrane protein. Treatment with antibiotics or antibodies against Sulcia outer membrane protein interferes with this interaction and strongly prevents viral transmission to insect offspring. This newly discovered virus–bacterium interaction represents the first evidence that a viral pathogen can directly exploit a symbiotic bacterium for its transmission. We believe that such a model of virus–bacterium communication is a common phenomenon in nature.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: RDV moved with Sulcia bacteria into the oocyte of female N. cincticeps.
Figure 2: Direct attachment of RDV particles to the envelope of Sulcia was mediated by specific interaction between the 15 nm domain of RDV P2 and the BSA domain of Sulcia OMP.
Figure 3: Effects of rifampicin treatment on bacterial symbionts and life history of N. cincticeps.

Similar content being viewed by others

References

  1. Gray, S. M. & Banerjee, N. Mechanisms of arthropod transmission of plant and animal viruses. Microbiol. Mol. Biol. Rev. 63, 128–148 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Baumann, P. Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155–189 (2005).

    Article  CAS  Google Scholar 

  3. Feldhaar, H. Bacterial symbionts as mediators of ecologically important traits of insect host. Ecol. Entomol. 36, 533–543 (2011).

    Article  Google Scholar 

  4. Martinez, J. et al. Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog. 10, e1004369 (2014).

    Article  Google Scholar 

  5. Pinheiro, P. V., Kliot, A., Ghanim, M. & Cilia, M. Is there a role for symbiotic bacteria in plant virus transmission by insects? Curr. Opin. Insect Sci. 8, 69–78 (2015).

    Article  Google Scholar 

  6. Koga, R., Bennett, G. M., Cryan, J. R. & Moran, N. A. Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 15, 2073–2081 (2013).

    Article  Google Scholar 

  7. Noda, H. et al. Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: cicadellidae). Appl. Entomol. Zool. 47, 217–225 (2012).

    Article  CAS  Google Scholar 

  8. Hibino, H. Biology and epidemiology of rice viruses. Annu. Rev. Phytopathol. 34, 249–274 (1996).

    Article  CAS  Google Scholar 

  9. Koga, R., Meng, X. Y., Tsuchida, T. & Fukatsu, T. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface. Proc. Natl Acad. Sci. USA. 109, E1230–E1237 (2012).

    Article  CAS  Google Scholar 

  10. Huo, Y. et al. Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. PLoS Pathog. 10, e1003949 (2014).

    Article  Google Scholar 

  11. Hogenhout, S. A., Ammar, E. D., Whitfield, A. E. & Redinbaugh, M. G. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46, 327–359 (2008).

    Article  CAS  Google Scholar 

  12. Fukushi, T. Transmission of the virus through the eggs of an insect vector. Proc. Inme. Acad. 9, 457–460 (1933).

    Article  Google Scholar 

  13. Nasu, S. Electron microscopic studies on transovarial passage of rice dwarf virus. Jpn J. Appl. Entomol. Zool. 9, 225–237 (1965).

    Article  Google Scholar 

  14. Chen, Q. et al. Tubular structure induced by a plant virus facilitates viral spread in its vector insect. PLoS Pathog. 8, e1003032 (2012).

    Article  CAS  Google Scholar 

  15. Moran, N., Tran, P. & Gerardo, N. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Environ. Microbiol. 71, 8802–8810 (2005).

    Article  CAS  Google Scholar 

  16. Miyazaki, N. et al. Electron microscopic imaging revealed the flexible filamentous structure of the cell attachment protein P2 of rice dwarf virus located around the icosahedral 5-fold axes. J. Biochem. 159, 181–190 (2016).

    Article  CAS  Google Scholar 

  17. Orlova, E. V. How viruses infect bacteria? EMBO J. 28, 797–798 (2009).

    Article  CAS  Google Scholar 

  18. Honda, K. et al. Retention of rice dwarf virus by descendants of pairs of viruliferous vector insects after rearing for 6 years. Phytopathology 97, 712–716 (2007).

    Article  Google Scholar 

  19. Bennett, G. M. & Moran, N. A. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc. Natl Acad. Sci. USA. 112, 10169–10176 (2015).

    Article  CAS  Google Scholar 

  20. Chang, H. H. et al. Complete genome sequence of ‘Candidatus Sulcia muelleri’ ML, an obligate nutritional symbiont of maize leafhopper (Dalbulus maidis). Genome Announc. 3, e01483–14 (2015).

    PubMed  PubMed Central  Google Scholar 

  21. Brasset, E. et al. Viral particles of the endogenous retrovirus ZAM from Drosophila melanogaster use a pre-existing endosome/exosome pathway for transfer to the oocyte. Retrovirology 3, 25 (2006).

    Article  CAS  Google Scholar 

  22. Márquez, L. M., Redman, R. S., Rodriguez, R. J. & Roossinck, M. J. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315, 513–515 (2007).

    Article  Google Scholar 

  23. Vautrin, E. & Vavre, F. Interactions between vertically transmitted symbionts: cooperation or conflict? Trends Microbiol. 17, 95–99 (2009).

    Article  CAS  Google Scholar 

  24. Wei, T., Chen, H., Ichiki-Uehara, T., Hibino, H. & Omura, T. Entry of rice dwarf virus into cultured cells of its insect vector involves clathrin-mediated endocytosis. J. Virol. 81, 7811–7815 (2007).

    Article  CAS  Google Scholar 

  25. Jia, D. et al. Development of an insect vector cell culture and RNA interference system to investigate the functional role of Fijivirus replication protein. J. Virol. 86, 5800–5807 (2012).

    Article  CAS  Google Scholar 

  26. Omura, T., Morinaka, T., Inoue, H. & Saito, Y. Purification and some properties of rice gall dwarf virus, a new phytoreovirus. Phytopathology 72, 1246–1249 (1982).

    Article  Google Scholar 

  27. Liu, S., Ding, Z., Zhang, C., Yang, B. & Liu, Z. Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochem. Mol. Biol. 40, 666–671 (2010).

    Article  CAS  Google Scholar 

  28. Lane, H. A. & Nigg, E. A. Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J. Cell Biol. 135, 1701–1713 (1996).

    Article  CAS  Google Scholar 

  29. Noda, H., Koizumi, Y., Zhang, Q. & Deng, K. J. Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem. Mol. Biol. 31, 727–737 (2001).

    Article  CAS  Google Scholar 

  30. Lan, H. et al. Small interfering RNA pathway modulates initial viral infection in midgut epithelium of insect after ingestion of virus. J. Virol. 90, 917–929 (2016).

    Article  CAS  Google Scholar 

  31. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Science Foundation for Outstanding Youth (grant no. 31325023), the National Basic Research Program of China (973 Program, no. 2014CB138400), the National Natural Science Foundation of China (grant no. 31571979) and the FAFU Foundation for Outstanding Youth (grant no. XJQ201507).

Author information

Authors and Affiliations

Authors

Contributions

All authors read and approved the manuscript. D.J., Q.M., Y.C., Y.Li and T.W. conceived and designed the study, and wrote the paper. D.J., Q.M. and Y.C. contributed equally to this work, performed most experiments and helped with data analysis. Y.Liu and H.C. performed the transmission electron microscopy. W.W. and X.Z. performed gene cloning and immunoprecipitation. Q.C. performed RT–qPCR experiments. Y.Li and T.W. discussed the data and revised the manuscript. T.W. and Y.Li organized and directed the project.

Corresponding authors

Correspondence to Yi Li or Taiyun Wei.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–5 (PDF 968 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, D., Mao, Q., Chen, Y. et al. Insect symbiotic bacteria harbour viral pathogens for transovarial transmission. Nat Microbiol 2, 17025 (2017). https://doi.org/10.1038/nmicrobiol.2017.25

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nmicrobiol.2017.25

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing