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 Onder, Dorcas 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


Drosophila melanogaster is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described in association with the Drosophilidae. This has limited the opportunity to use natural host-pathogen combinations in experimental studies, and may have biased our understanding of the Drosophila virome. Here we describe fourteen DNA viruses detectable by metagenomic analysis of 6.5 thousand pool-sequenced Drosophila, sampled from 47 European locations between 2014 and 2016. These include three new Nudiviruses, a new and divergent Entomopox virus, 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, an RNA Partitivirus, segregating at very low frequency. Remarkably, we show that Vesanto virus, a small DNA virus previously described as a Bidnavirus, may be composed of up to 12 segments and represents a new lineage of segmented DNA viruses. Only two of the DNA viruses, Kallithea virus (Nudiviridae) and Vesanto virus (Bidna-virus like) are common, being found in 2% or more of wild flies. The other viruses are rare, with many likely to be represented by a single infected fly in the collection. We find that virus prevalence in Europe reflects that seen in publicly-available datasets, with Kallithea virus and Vesanto virus being commonly detectable in data from wild-caught flies and large population cages, and the others being rare or absent. These analyses suggest that DNA viruses are generally rarer than RNA viruses in D. melanogaster, and may be less likely to persist in laboratory cultures. Our findings go some way to redress the 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.