<italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>

ABSTRACT The endosymbiotic bacteria of the genus Wolbachia are present in most insects and are maternally transmitted through the germline. Moreover, these intracellular bacteria exert antiviral activity against insect RNA viruses, as in Drosophila melanogaster, which could explain the prevalence of...

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Autores principales: Franck Touret, François Guiguen, Christophe Terzian
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:a321f2997c5e4b8fa90402da28a68f7f2021-11-15T15:45:54Z<italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>10.1128/mBio.01529-142150-7511https://doaj.org/article/a321f2997c5e4b8fa90402da28a68f7f2014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01529-14https://doaj.org/toc/2150-7511ABSTRACT The endosymbiotic bacteria of the genus Wolbachia are present in most insects and are maternally transmitted through the germline. Moreover, these intracellular bacteria exert antiviral activity against insect RNA viruses, as in Drosophila melanogaster, which could explain the prevalence of Wolbachia bacteria in natural populations. Wolbachia is maternally transmitted in D. melanogaster through a mechanism that involves distribution at the posterior pole of mature oocytes and then incorporation into the pole cells of the embryos. In parallel, maternal transmission of several endogenous retroviruses is well documented in D. melanogaster. Notably, gypsy retrovirus is expressed in permissive follicle cells and transferred to the oocyte and then to the offspring by integrating into their genomes. Here, we show that the presence of Wolbachia wMel reduces the rate of gypsy insertion into the ovo gene. However, the presence of Wolbachia does not modify the expression levels of gypsy RNA and envelope glycoprotein from either permissive or restrictive ovaries. Moreover, Wolbachia affects the pattern of distribution of the retroviral particles and the gypsy envelope protein in permissive follicle cells. Altogether, our results enlarge the knowledge of the antiviral activity of Wolbachia to include reducing the maternal transmission of endogenous retroviruses in D. melanogaster. IMPORTANCE Animals have established complex relationships with bacteria and viruses that spread horizontally among individuals or are vertically transmitted, i.e., from parents to offspring. It is well established that members of the genus Wolbachia, maternally inherited symbiotic bacteria present mainly in arthropods, reduce the replication of several RNA viruses transmitted horizontally. Here, we demonstrate for the first time that Wolbachia diminishes the maternal transmission of gypsy, an endogenous retrovirus in Drosophila melanogaster. We hypothesize that gypsy cannot efficiently integrate into the germ cells of offspring during embryonic development in the presence of Wolbachia because both are competitors for localization to the posterior pole of the egg. More generally, it would be of interest to analyze the influence of Wolbachia on vertically transmitted exogenous viruses, such as some arboviruses.Franck TouretFrançois GuiguenChristophe TerzianAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Franck Touret
François Guiguen
Christophe Terzian
<italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
description ABSTRACT The endosymbiotic bacteria of the genus Wolbachia are present in most insects and are maternally transmitted through the germline. Moreover, these intracellular bacteria exert antiviral activity against insect RNA viruses, as in Drosophila melanogaster, which could explain the prevalence of Wolbachia bacteria in natural populations. Wolbachia is maternally transmitted in D. melanogaster through a mechanism that involves distribution at the posterior pole of mature oocytes and then incorporation into the pole cells of the embryos. In parallel, maternal transmission of several endogenous retroviruses is well documented in D. melanogaster. Notably, gypsy retrovirus is expressed in permissive follicle cells and transferred to the oocyte and then to the offspring by integrating into their genomes. Here, we show that the presence of Wolbachia wMel reduces the rate of gypsy insertion into the ovo gene. However, the presence of Wolbachia does not modify the expression levels of gypsy RNA and envelope glycoprotein from either permissive or restrictive ovaries. Moreover, Wolbachia affects the pattern of distribution of the retroviral particles and the gypsy envelope protein in permissive follicle cells. Altogether, our results enlarge the knowledge of the antiviral activity of Wolbachia to include reducing the maternal transmission of endogenous retroviruses in D. melanogaster. IMPORTANCE Animals have established complex relationships with bacteria and viruses that spread horizontally among individuals or are vertically transmitted, i.e., from parents to offspring. It is well established that members of the genus Wolbachia, maternally inherited symbiotic bacteria present mainly in arthropods, reduce the replication of several RNA viruses transmitted horizontally. Here, we demonstrate for the first time that Wolbachia diminishes the maternal transmission of gypsy, an endogenous retrovirus in Drosophila melanogaster. We hypothesize that gypsy cannot efficiently integrate into the germ cells of offspring during embryonic development in the presence of Wolbachia because both are competitors for localization to the posterior pole of the egg. More generally, it would be of interest to analyze the influence of Wolbachia on vertically transmitted exogenous viruses, such as some arboviruses.
format article
author Franck Touret
François Guiguen
Christophe Terzian
author_facet Franck Touret
François Guiguen
Christophe Terzian
author_sort Franck Touret
title <italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_short <italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_full <italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_fullStr <italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_full_unstemmed <italic toggle="yes">Wolbachia</italic> Influences the Maternal Transmission of the <italic toggle="yes">gypsy</italic> Endogenous Retrovirus in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_sort <italic toggle="yes">wolbachia</italic> influences the maternal transmission of the <italic toggle="yes">gypsy</italic> endogenous retrovirus in <named-content content-type="genus-species">drosophila melanogaster</named-content>
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/a321f2997c5e4b8fa90402da28a68f7f
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