The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe

Megan A. Wallace, Kelsey A. Coffman, Clément Gilbert, Sanjana Ravindran, Gregory F. Albery, Jessica Abbott, Eliza Argyridou, Paola Bellosta, Andrea J. Betancourt, Hervé Colinet, Katarina Eric, Amanda Glaser-Schmitt, Sonja Grath, Mihailo Jelic, Maaria Kankare, Iryna Kozeretska, Volker Loeschcke, Catherine Montchamp-Moreau, Lino Ometto, Banu Sebnem OnderDorcas J. Orengo, John Parsch, Marta Pascual, Aleksandra Patenkovic, Eva Puerma, Michael G. Ritchie, Omar Rota-Stabelli, Mads Fristrup Schou, Svitlana V. Serga, Marina Stamenkovic-Radak, Marija Tanaskovic, Marija Savic Veselinovic, Jorge Vieira, Cristina P. Vieira, Martin Kapun, Thomas Flatt, Josefa González, Fabian Staubach, Darren J. Obbard*

*Corresponding author for this work

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Abstract

Drosophila melanogaster is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described from the family Drosophilidae. This deficiency limits our opportunity to use natural host-pathogen combinations in experimental studies, and may bias our understanding of the Drosophila virome. Here, we report fourteen DNA viruses detected in a metagenomic analysis of 6668 pool-sequenced Drosophila, sampled from forty-seven European locations between 2014 and 2016. These include three new nudiviruses, a new and divergent entomopoxvirus, a virus related to Leptopilina boulardi filamentous virus, and a virus related to Musca domestica salivary gland hypertrophy virus. We also find an endogenous genomic copy of galbut virus, a double-stranded RNA partitivirus, segregating at very low frequency. Remarkably, we find that Drosophila Vesanto virus, a small DNA virus previously described as a bidnavirus, may be composed of up to twelve segments and thus represent a new lineage of segmented DNA viruses. Two of the DNA viruses, Drosophila Kallithea nudivirus and Drosophila Vesanto virus are relatively common, found in 2 per cent or more of wild flies. The others are rare, with many likely to be represented by a single infected fly. We find that virus prevalence in Europe reflects the prevalence seen in publicly available datasets, with Drosophila Kallithea nudivirus and Drosophila Vesanto virus the only ones commonly detectable in public data from wild-caught flies and large population cages, and the other viruses being rare or absent. These analyses suggest that DNA viruses are at lower prevalence than RNA viruses in D.melanogaster, and may be less likely to persist in laboratory cultures. Our findings go some way to redressing an earlier bias toward RNA virus studies in Drosophila, and lay the foundation needed to harness the power of Drosophila as a model system for the study of DNA viruses.

Original languageEnglish
Article numberveab031
Number of pages23
JournalVirus Evolution
Volume7
Issue number1
Early online date1 Apr 2021
DOIs
Publication statusPublished - 1 Apr 2021

Keywords

  • Adintovirus
  • Bidnavirus
  • Densovirus
  • DNA virus
  • Drosophila
  • Endogenous viral element
  • Filamentous virus
  • Galbut virus
  • Nudivirus

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