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

Wallace, Megan A. ; Coffman, Kelsey A. ; Gilbert, Clément ; Ravindran, Sanjana ; Albery, Gregory F. ; Abbott, Jessica LU orcid ; Argyridou, Eliza ; Bellosta, Paola ; Betancourt, Andrea J. and Colinet, Hervé , et al. (2021) In Virus Evolution 7(1).
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... (More)

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.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
adintovirus, bidnavirus, densovirus, DNA virus, Drosophila, endogenous viral element, filamentous virus, galbut virus, nudivirus
in
Virus Evolution
volume
7
issue
1
article number
veab031
publisher
Oxford University Press
external identifiers
  • scopus:85114635292
  • pmid:34408913
ISSN
2057-1577
DOI
10.1093/ve/veab031
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2021 The Author(s) 2021. Published by Oxford University Press.
id
e7018af4-f85b-4fe1-821e-37f78a06d250
date added to LUP
2021-10-18 10:53:26
date last changed
2024-06-15 18:15:43
@article{e7018af4-f85b-4fe1-821e-37f78a06d250,
  abstract     = {{<p>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.</p>}},
  author       = {{Wallace, Megan A. and Coffman, Kelsey A. and Gilbert, Clément and Ravindran, Sanjana and Albery, Gregory F. and Abbott, Jessica and Argyridou, Eliza and Bellosta, Paola and Betancourt, Andrea J. and Colinet, Hervé and Eric, Katarina and Glaser-Schmitt, Amanda and Grath, Sonja and Jelic, Mihailo and Kankare, Maaria and Kozeretska, Iryna and Loeschcke, Volker and Montchamp-Moreau, Catherine and Ometto, Lino and Onder, Banu Sebnem and Orengo, Dorcas J. and Parsch, John and Pascual, Marta and Patenkovic, Aleksandra and Puerma, Eva and Ritchie, Michael G. and Rota-Stabelli, Omar and Schou, Mads Fristrup and Serga, Svitlana V. and Stamenkovic-Radak, Marina and Tanaskovic, Marija and Veselinovic, Marija Savic and Vieira, Jorge and Vieira, Cristina P. and Kapun, Martin and Flatt, Thomas and González, Josefa and Staubach, Fabian and Obbard, Darren J.}},
  issn         = {{2057-1577}},
  keywords     = {{adintovirus; bidnavirus; densovirus; DNA virus; Drosophila; endogenous viral element; filamentous virus; galbut virus; nudivirus}},
  language     = {{eng}},
  month        = {{01}},
  number       = {{1}},
  publisher    = {{Oxford University Press}},
  series       = {{Virus Evolution}},
  title        = {{The discovery, distribution, and diversity of DNA viruses associated with Drosophila melanogaster in Europe}},
  url          = {{http://dx.doi.org/10.1093/ve/veab031}},
  doi          = {{10.1093/ve/veab031}},
  volume       = {{7}},
  year         = {{2021}},
}