title: The Discovery, Distribution, and Evolution of Viruses Associated with Drosophila melanogaster.
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 >2,000 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.
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Claire L
authors.initials: CL
authors.lastname: Webster
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Fergal M
authors.initials: FM
authors.lastname: Waldron
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Shaun
authors.initials: S
authors.lastname: Robertson
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Daisy
authors.initials: D
authors.lastname: Crowson
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Giada
authors.initials: G
authors.lastname: Ferrari
authors.affiliation: Institute of Immunity and Infection Research, and the Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Juan F
authors.initials: JF
authors.lastname: Quintana
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Brouqui
authors.affiliation: Institute of Cell Biology, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Elizabeth H
authors.initials: EH
authors.lastname: Bayne
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Ben
authors.initials: B
authors.lastname: Longdon
authors.affiliation: Institute of Immunity and Infection Research, and the Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Amy H
authors.initials: AH
authors.lastname: Buck
authors.affiliation: Department of Entomology, Cornell University, Ithaca, New York, United States of America.
authors.forename: Brian P
authors.initials: BP
authors.lastname: Lazzaro
authors.affiliation: Department of Parasitology, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, Ghana.
authors.forename: Jewelna
authors.initials: J
authors.lastname: Akorli
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Penelope R
authors.initials: PR
authors.lastname: Haddrill
authors.affiliation: Institute of Evolutionary Biology and Centre for Immunity Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Darren J
authors.initials: DJ
authors.lastname: Obbard
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D005075:Biological Evolution; D017124:Conserved Sequence; D004331:Drosophila melanogaster / Q000821:virology*; D000067636:Drosophila simulans / Q000821:virology; D005260:Female; D008297:Male; D056186:Metagenomics; D008969:Molecular Sequence Data; D012313:RNA / Q000032:analysis; D034622:RNA Interference; D014764:Viral Proteins / Q000737:chemistry; D020577:Wolbachia / Q000302:isolation & purification
chemical_list: D014764:Viral Proteins; D012313:RNA