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

doi:10.1093/ve/veab031

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 af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

18 Citationer (Scopus)

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.

Originalsprog	Engelsk
Artikelnummer	veab031
Tidsskrift	Virus evolution
Vol/bind	7
Nummer	1
ISSN	2057-1577
DOI	https://doi.org/10.1093/ve/veab031
Status	Udgivet - jan. 2021

Adgang til dokumentet

10.1093/ve/veab031Licens: CC BY

Andre filer og links

Link to publication in Scopus

Citationsformater

Wallace, M. A., Coffman, K. A., Gilbert, C., Ravindran, S., Albery, G. F., Abbott, J., Argyridou, E., Bellosta, P., Betancourt, A. J., Colinet, H., Eric, K., Glaser-Schmitt, A., Grath, S., Jelic, M., Kankare, M., Kozeretska, I., Loeschcke, V., Montchamp-Moreau, C., Ometto, L., ... Obbard, D. J. (2021). The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe. Virus evolution, 7(1), Artikel veab031. https://doi.org/10.1093/ve/veab031

@article{a468e8c52ac044de9b90231be650eef2,

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

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.",

keywords = "adintovirus, bidnavirus, densovirus, DNA virus, Drosophila, endogenous viral element, filamentous virus, galbut virus, nudivirus",

author = "Wallace, {Megan A.} and Coffman, {Kelsey A.} and Cl{\'e}ment Gilbert and Sanjana Ravindran and Albery, {Gregory F.} and Jessica Abbott and Eliza Argyridou and Paola Bellosta and Betancourt, {Andrea J.} and Herv{\'e} Colinet and Katarina Eric and Amanda Glaser-Schmitt and Sonja Grath and Mihailo Jelic and Maaria Kankare and Iryna Kozeretska and Volker Loeschcke and Catherine Montchamp-Moreau and Lino Ometto and Onder, {Banu Sebnem} and Orengo, {Dorcas J.} and John Parsch and Marta Pascual and Aleksandra Patenkovic and Eva Puerma and Ritchie, {Michael G.} and Omar Rota-Stabelli and Schou, {Mads Fristrup} and Serga, {Svitlana V.} and Marina Stamenkovic-Radak and Marija Tanaskovic and Veselinovic, {Marija Savic} and Jorge Vieira and Vieira, {Cristina P.} and Martin Kapun and Thomas Flatt and Josefa Gonz{\'a}lez and Fabian Staubach and Obbard, {Darren J.}",

note = "Publisher Copyright: {\textcopyright} 2021 The Author(s) 2021. Published by Oxford University Press.",

year = "2021",

month = jan,

doi = "10.1093/ve/veab031",

language = "English",

volume = "7",

journal = "Virus evolution",

issn = "2057-1577",

publisher = "Oxford University Press",

number = "1",

}

Wallace, MA, Coffman, KA, Gilbert, C, Ravindran, S, Albery, GF, Abbott, J, Argyridou, E, Bellosta, P, Betancourt, AJ, Colinet, H, Eric, K, Glaser-Schmitt, A, Grath, S, Jelic, M, Kankare, M, Kozeretska, I, Loeschcke, V, Montchamp-Moreau, C, Ometto, L, Onder, BS, Orengo, DJ, Parsch, J, Pascual, M, Patenkovic, A, Puerma, E, Ritchie, MG, Rota-Stabelli, O, Schou, MF, Serga, SV, Stamenkovic-Radak, M, Tanaskovic, M, Veselinovic, MS, Vieira, J, Vieira, CP, Kapun, M, Flatt, T, González, J, Staubach, F & Obbard, DJ 2021, 'The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe', Virus evolution, bind 7, nr. 1, veab031. https://doi.org/10.1093/ve/veab031

TY - JOUR

T1 - The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe

AU - Wallace, Megan A.

AU - Coffman, Kelsey A.

AU - Gilbert, Clément

AU - Ravindran, Sanjana

AU - Albery, Gregory F.

AU - Abbott, Jessica

AU - Argyridou, Eliza

AU - Bellosta, Paola

AU - Betancourt, Andrea J.

AU - Colinet, Hervé

AU - Eric, Katarina

AU - Glaser-Schmitt, Amanda

AU - Grath, Sonja

AU - Jelic, Mihailo

AU - Kankare, Maaria

AU - Kozeretska, Iryna

AU - Loeschcke, Volker

AU - Montchamp-Moreau, Catherine

AU - Ometto, Lino

AU - Onder, Banu Sebnem

AU - Orengo, Dorcas J.

AU - Parsch, John

AU - Pascual, Marta

AU - Patenkovic, Aleksandra

AU - Puerma, Eva

AU - Ritchie, Michael G.

AU - Rota-Stabelli, Omar

AU - Schou, Mads Fristrup

AU - Serga, Svitlana V.

AU - Stamenkovic-Radak, Marina

AU - Tanaskovic, Marija

AU - Veselinovic, Marija Savic

AU - Vieira, Jorge

AU - Vieira, Cristina P.

AU - Kapun, Martin

AU - Flatt, Thomas

AU - González, Josefa

AU - Staubach, Fabian

AU - Obbard, Darren J.

PY - 2021/1

Y1 - 2021/1

N2 - 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.

AB - 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.

KW - adintovirus

KW - bidnavirus

KW - densovirus

KW - DNA virus

KW - Drosophila

KW - endogenous viral element

KW - filamentous virus

KW - galbut virus

KW - nudivirus

UR - http://www.scopus.com/inward/record.url?scp=85114635292&partnerID=8YFLogxK

U2 - 10.1093/ve/veab031

DO - 10.1093/ve/veab031

M3 - Journal article

C2 - 34408913

AN - SCOPUS:85114635292

SN - 2057-1577

VL - 7

JO - Virus evolution

JF - Virus evolution

IS - 1

M1 - veab031

ER -

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

Abstract

Adgang til dokumentet

Andre filer og links

Fingeraftryk

Citationsformater