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

View ORCID ProfileMegan A. Wallace, View ORCID ProfileKelsey A. Coffman, View ORCID ProfileClément Gilbert, View ORCID ProfileSanjana Ravindran, View ORCID ProfileGregory F. Albery, View ORCID ProfileJessica Abbott, View ORCID ProfileEliza Argyridou, View ORCID ProfilePaola Bellosta, View ORCID ProfileAndrea J. Betancourt, View ORCID ProfileHervé Colinet, View ORCID ProfileKatarina Eric, View ORCID ProfileAmanda Glaser-Schmitt, View ORCID ProfileSonja Grath, View ORCID ProfileMihailo Jelic, View ORCID ProfileMaaria Kankare, View ORCID ProfileIryna Kozeretska, View ORCID ProfileVolker Loeschcke, View ORCID ProfileCatherine Montchamp-Moreau, View ORCID ProfileLino Ometto, View ORCID ProfileBanu Sebnem Onder, View ORCID ProfileDorcas J. Orengo, View ORCID ProfileJohn Parsch, View ORCID ProfileMarta Pascual, View ORCID ProfileAleksandra Patenkovic, View ORCID ProfileEva Puerma, View ORCID ProfileMichael G. Ritchie, View ORCID ProfileOmar Rota-Stabelli, View ORCID ProfileMads Fristrup Schou, View ORCID ProfileSvitlana V. Serga, View ORCID ProfileMarina Stamenkovic-Radak, View ORCID ProfileMarija Tanaskovic, View ORCID ProfileMarija Savic Veselinovic, View ORCID ProfileJorge Vieira, View ORCID ProfileCristina P. Vieira, View ORCID ProfileMartin Kapun, View ORCID ProfileThomas Flatt, View ORCID ProfileJosefa González, View ORCID ProfileFabian Staubach, View ORCID ProfileDarren J. Obbard
doi: https://doi.org/10.1101/2020.10.16.342956
Megan A. Wallace
1The European Drosophila Population Genomics Consortium (DrosEU)
2Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, Charlotte Auerbach Road, Edinburgh, EH9 3FL, UK
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  • ORCID record for Megan A. Wallace
Kelsey A. Coffman
3Department of Entomology, University of Georgia, Athens, Georgia, USA
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  • ORCID record for Kelsey A. Coffman
Clément Gilbert
1The European Drosophila Population Genomics Consortium (DrosEU)
4Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198 Gif-sur-Yvette, France
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  • ORCID record for Clément Gilbert
Sanjana Ravindran
2Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, Charlotte Auerbach Road, Edinburgh, EH9 3FL, UK
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  • ORCID record for Sanjana Ravindran
Gregory F. Albery
5Department of Biology, Georgetown University, Washington DC, USA
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  • ORCID record for Gregory F. Albery
Jessica Abbott
1The European Drosophila Population Genomics Consortium (DrosEU)
6Department of Biology, Section for Evolutionary Ecology, Lund University, Sölvegatan 37, 223 62 Lund, Sweden
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  • ORCID record for Jessica Abbott
Eliza Argyridou
1The European Drosophila Population Genomics Consortium (DrosEU)
7Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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  • ORCID record for Eliza Argyridou
Paola Bellosta
1The European Drosophila Population Genomics Consortium (DrosEU)
8Dept of Cellular, Computational and Integrative Biology - CIBIO University of Trento, Via Sommarive 9, 38123 Trento, Italy
9Dept of Medicine & Endocrinology, NYU Langone Medical Center, 550 First Ave, 10016 NY USA
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Andrea J. Betancourt
1The European Drosophila Population Genomics Consortium (DrosEU)
10Institute of Integrative Biology, University of Liverpool, Liverpool, L69 7ZB, UK
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Hervé Colinet
1The European Drosophila Population Genomics Consortium (DrosEU)
11UMR CNRS 6553 ECOBIO, Université de Rennes1, France
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Katarina Eric
1The European Drosophila Population Genomics Consortium (DrosEU)
12University of Belgrade, Institute for Biological Research “Sinisa Stankovic”, National Institute of Republic of Serbia, Bulevar despota Stefana 142 Belgrade, Serbia
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Amanda Glaser-Schmitt
1The European Drosophila Population Genomics Consortium (DrosEU)
7Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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  • ORCID record for Amanda Glaser-Schmitt
Sonja Grath
1The European Drosophila Population Genomics Consortium (DrosEU)
7Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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Mihailo Jelic
1The European Drosophila Population Genomics Consortium (DrosEU)
13University of Belgrade – Faculty of Biology, Studentski trg 16, Belgrade, Serbia
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  • ORCID record for Mihailo Jelic
Maaria Kankare
1The European Drosophila Population Genomics Consortium (DrosEU)
14Department of Biological and Environmental Science, University of Jyväskylä, Finland
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  • ORCID record for Maaria Kankare
Iryna Kozeretska
1The European Drosophila Population Genomics Consortium (DrosEU)
15National Antarctic Scientific Center of Ukraine, 16 Shevchenko Ave., 01601, Kyiv, Ukraine
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  • ORCID record for Iryna Kozeretska
Volker Loeschcke
1The European Drosophila Population Genomics Consortium (DrosEU)
16Dept. of Biology, Genetics, Ecology and Evolution, Aarhus University, Ny Munkegade 116, DK-8000 Aarhus C, Denmark
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Catherine Montchamp-Moreau
1The European Drosophila Population Genomics Consortium (DrosEU)
4Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198 Gif-sur-Yvette, France
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  • ORCID record for Catherine Montchamp-Moreau
Lino Ometto
1The European Drosophila Population Genomics Consortium (DrosEU)
17Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, Italy
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Banu Sebnem Onder
1The European Drosophila Population Genomics Consortium (DrosEU)
18Department of Biology, Faculty of Science, Hacettepe University, Ankara, Turkey
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Dorcas J. Orengo
1The European Drosophila Population Genomics Consortium (DrosEU)
19Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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John Parsch
1The European Drosophila Population Genomics Consortium (DrosEU)
7Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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Marta Pascual
1The European Drosophila Population Genomics Consortium (DrosEU)
19Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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Aleksandra Patenkovic
1The European Drosophila Population Genomics Consortium (DrosEU)
12University of Belgrade, Institute for Biological Research “Sinisa Stankovic”, National Institute of Republic of Serbia, Bulevar despota Stefana 142 Belgrade, Serbia
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Eva Puerma
1The European Drosophila Population Genomics Consortium (DrosEU)
19Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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Michael G. Ritchie
1The European Drosophila Population Genomics Consortium (DrosEU)
20Centre for Biological Diversity, St Andrews University, St Andrews, Scotland HY15 4SS UK
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Omar Rota-Stabelli
1The European Drosophila Population Genomics Consortium (DrosEU)
21Research and Innovation Center, Fondazione E. Mach, 38010, San Michele all’Adige(TN), Italy
22Centre Agriculture Food Environment, University of Trento, 38010, San Michele all’Adige(TN), Italy
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Mads Fristrup Schou
1The European Drosophila Population Genomics Consortium (DrosEU)
6Department of Biology, Section for Evolutionary Ecology, Lund University, Sölvegatan 37, 223 62 Lund, Sweden
23Department of Bioscience, Aarhus University, Aarhus, Denmark
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Svitlana V. Serga
1The European Drosophila Population Genomics Consortium (DrosEU)
15National Antarctic Scientific Center of Ukraine, 16 Shevchenko Ave., 01601, Kyiv, Ukraine
24Taras Shevchenko National University of Kyiv, 01601, 64 Volodymyrska str, Kyiv, Ukraine
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Marina Stamenkovic-Radak
1The European Drosophila Population Genomics Consortium (DrosEU)
13University of Belgrade – Faculty of Biology, Studentski trg 16, Belgrade, Serbia
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Marija Tanaskovic
1The European Drosophila Population Genomics Consortium (DrosEU)
12University of Belgrade, Institute for Biological Research “Sinisa Stankovic”, National Institute of Republic of Serbia, Bulevar despota Stefana 142 Belgrade, Serbia
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Marija Savic Veselinovic
1The European Drosophila Population Genomics Consortium (DrosEU)
13University of Belgrade – Faculty of Biology, Studentski trg 16, Belgrade, Serbia
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Jorge Vieira
1The European Drosophila Population Genomics Consortium (DrosEU)
25Instituto de Biologia Molecular e Celular (IBMC), University of Porto, Porto, Portugal
26i3S-Instituto de Investigação e Inovação em Saúde, University of Porto, Porto, Portugal
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Cristina P. Vieira
1The European Drosophila Population Genomics Consortium (DrosEU)
25Instituto de Biologia Molecular e Celular (IBMC), University of Porto, Porto, Portugal
26i3S-Instituto de Investigação e Inovação em Saúde, University of Porto, Porto, Portugal
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Martin Kapun
1The European Drosophila Population Genomics Consortium (DrosEU)
27Department of Evolutionary Biology and Environmental Studies, University of Zürich, Switzerland; Division of Cell & Developmental Biology, Medical University of Vienna, Austria
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Thomas Flatt
1The European Drosophila Population Genomics Consortium (DrosEU)
28Department of Biology, University of Fribourg, CH-1700 Fribourg, Switzerland
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Josefa González
1The European Drosophila Population Genomics Consortium (DrosEU)
29Institute of Evolutionary Biology (CSIC-UPF), Barcelona, Spain
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Fabian Staubach
1The European Drosophila Population Genomics Consortium (DrosEU)
30Department of Evolution and Ecology, University of Freiburg, 79104 Freiburg, Germany
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Darren J. Obbard
1The European Drosophila Population Genomics Consortium (DrosEU)
2Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, Charlotte Auerbach Road, Edinburgh, EH9 3FL, UK
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  • For correspondence: darren.obbard@ed.ac.uk
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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 approximately 6500 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, a dsRNA 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 12 segments and 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% 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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • megan.wallace{at}ed.ac.uk, kcoffman{at}uga.edu, clement.gilbert{at}egce.cnrs-gif.fr, sanjana.ravindran{at}ed.ac.uk, gfalbery{at}gmail.com, jessica.abbott{at}biol.lu.se, argyridou{at}bio.lmu.de, paola.bellosta{at}unitn.it, A.Betancourt{at}liverpool.ac.uk, herve.colinet{at}univ-rennes1.fr, katarina.eric{at}ibiss.bg.ac.rs, glaser{at}bio.lmu.de, grath{at}bio.lmu.de, mihailoj{at}bio.bg.ac.rs, maaria.kankare{at}jyu.fi, iryna.kozeretska{at}gmail.com, volker{at}bios.au.dk, Catherine.Montchamp{at}egce.cnrs-gif.fr, lino.ometto{at}unipv.it, bdalgic{at}hacettepe.edu.tr, dorcasorengo{at}ub.edu, parsch{at}bio.lmu.de, martapascual{at}ub.edu, aleksandra{at}ibiss.bg.ac.rs, e.puerma{at}ub.edu, mgr{at}st-andrews.ac.uk, omar.rota{at}fmach.it, mads.schou{at}biol.lu.se, svitlana.serga{at}gmail.com, marina{at}bio.bg.ac.rs, marija.tanaskovic{at}ibiss.bg.ac.rs, marijas{at}bio.bg.ac.rs, jbvieira{at}ibmc.up.pt, cgvieira{at}ibmc.up.pt, martin.kapun{at}uzh.ch, thomas.flatt{at}unifr.ch, josefa.gonzalez{at}csic.es, fabian.staubach{at}biologie.uni-freiburg.de

  • https://doi.org/10.6084/m9.figshare.14161250.v1

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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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
bioRxiv 2020.10.16.342956; doi: https://doi.org/10.1101/2020.10.16.342956
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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
bioRxiv 2020.10.16.342956; doi: https://doi.org/10.1101/2020.10.16.342956

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