The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster

Claire L. Webster, Fergal M. Waldron, Shaun Robertson, Daisy Crowson, Giada Ferrari, Juan F. Quintana, Jean-Michel Brouqui, Elizabeth H. Bayne, Ben Longdon, Amy H. Buck, Brian P. Lazzaro, Jewelna Akorli, Penelope R. Haddrill, Darren J. Obbard

Research output: Contribution to journalArticle

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Abstract

Drosophila melanogaster is a valuable invertebrate model for viral infection and antiviral immunity, and is a focus for studies of insect-virus coevolution. Here we use a metagenomic approach to identify more than 20 previously undetected RNA viruses and a DNA virus associated with wild D. melanogaster. These viruses not only include distant relatives of known insect pathogens, but also novel groups of insect-infecting viruses. By sequencing virus-derived small RNAs we show that the viruses represent active infections of Drosophila. We find that the RNA viruses differ in the number and properties of their small RNAs, and we detect both siRNAs and a novel miRNA from the DNA virus. Analysis of small RNAs also allows us to identify putative viral sequences that lack detectable sequence similarity to known viruses. By surveying >2000 individually collected wild adult Drosophila we show that more than 30% of D. melanogaster carry a detectable virus, and more than 6% carry multiple viruses. However, despite a high prevalence of the Wolbachia endosymbiont—which is known to be protective against virus infections in Drosophila—we were unable to detect any relationship between the presence of Wolbachia and the presence of any virus. Using publicly available RNA-seq datasets we show that the community of viruses in Drosophila laboratories is very different from that seen in the wild, but that some of the newly discovered viruses are nevertheless widespread in laboratory lines and are ubiquitous in cell culture. By sequencing viruses from individual wild-collected flies we show that some viruses are shared between D. melanogaster and D. simulans. Our results provide an essential evolutionary and ecological context for host-virus interaction in Drosophila, and the newly reported viral sequences will help develop D. melanogaster further as a model for molecular and evolutionary virus research.
LanguageEnglish
Pages1-33
Number of pages33
JournalPLOS Biology
Volume13
Issue number7
DOIs
Publication statusPublished - 14 Jul 2015

Fingerprint

Drosophila melanogaster
Viruses
viruses
Drosophila
RNA Viruses
Insect Viruses
Wolbachia
RNA
insect viruses
DNA Viruses
DNA viruses
Virus Diseases
Metagenomics
infection
Molecular Models
molecular models
Invertebrates
entomopathogens
MicroRNAs
Diptera

Keywords

  • drosophila melanogaster
  • insect-virus coevolution
  • DNA
  • RNA
  • metagenomic approach
  • host-virus interaction

Cite this

Webster, C. L., Waldron, F. M., Robertson, S., Crowson, D., Ferrari, G., Quintana, J. F., ... Obbard, D. J. (2015). The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLOS Biology, 13(7), 1-33. https://doi.org/10.1371/journal.pbio.1002210
Webster, Claire L. ; Waldron, Fergal M. ; Robertson, Shaun ; Crowson, Daisy ; Ferrari, Giada ; Quintana, Juan F. ; Brouqui, Jean-Michel ; Bayne, Elizabeth H. ; Longdon, Ben ; Buck, Amy H. ; Lazzaro, Brian P. ; Akorli, Jewelna ; Haddrill, Penelope R. ; Obbard, Darren J. / The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. In: PLOS Biology. 2015 ; Vol. 13, No. 7. pp. 1-33.
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Webster, CL, Waldron, FM, Robertson, S, Crowson, D, Ferrari, G, Quintana, JF, Brouqui, J-M, Bayne, EH, Longdon, B, Buck, AH, Lazzaro, BP, Akorli, J, Haddrill, PR & Obbard, DJ 2015, 'The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster' PLOS Biology, vol. 13, no. 7, pp. 1-33. https://doi.org/10.1371/journal.pbio.1002210

The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. / Webster, Claire L.; Waldron, Fergal M.; Robertson, Shaun; Crowson, Daisy; Ferrari, Giada; Quintana, Juan F.; Brouqui, Jean-Michel; Bayne, Elizabeth H.; Longdon, Ben; Buck, Amy H.; Lazzaro, Brian P.; Akorli, Jewelna; Haddrill, Penelope R.; Obbard, Darren J.

In: PLOS Biology, Vol. 13, No. 7, 14.07.2015, p. 1-33.

Research output: Contribution to journalArticle

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AU - Quintana, Juan F.

AU - Brouqui, Jean-Michel

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AU - Haddrill, Penelope R.

AU - Obbard, Darren J.

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Webster CL, Waldron FM, Robertson S, Crowson D, Ferrari G, Quintana JF et al. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLOS Biology. 2015 Jul 14;13(7):1-33. https://doi.org/10.1371/journal.pbio.1002210