The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe
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. ; M.W. was supported by the UK Natural Environmental Research Council through the E3 doctoral training programme (NE/L002558/1), and S.R. was supported by Wellcome Trust PhD programme (108905/Z/15/Z). A.B. received funding from BBSRC (grant number BB/P00685X/1). T.F. received funding from Swiss National Science Foundation (grant numbers 31003A-182262, PP00P3_165836, and PP00P3_133641/1). C.G. received funding from Agence Nationale de la Recherche (grant number ANR-15-CE32-0011-01). J.G. received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (H2020-ERC-2014-CoG-647900) and from the Fundación Española para la Ciencia y la Tecnologia-Ministerio de Economía y Competitividad (FCT-15-10187). S.G. received funding from Deutsche Forschungsgemeinschaft (grant number GR 4495/2). M.K. received funding from Academy of Finland projects (268214 and 322980). M.K. received funding from Austrian Science Fund (FWF; grant number P32275). V.L. received funding from Danish Research council for natural Sciences (FNU; grant number 4002-00113B). B.S.O. received funding from the Scientific and Technological Research Council of Turkey (TUBITAK; grant number 214Z238). J.P. received funding from Deutsche Forschungsgemeinschaft (grant number PA 903/8). M.S.-R., M.S.V., and M.J. received funding from the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant number 451-03-68/2020-14/200178). F.S. received funding from Deutsche Forschungsgemeinschaft (grant number STA1154/4-1; Projektnummer 408908608). M.T., A.P., and K.E. received funding from the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant number 451-03-68/2020-14/200007). The DrosEU consortium has been funded by a Special Topics Network (STN) grant by the European Society of Evolutionary Biology (ESEB). ; Peer reviewed