The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>

ABSTRACT Insects commonly harbor facultative bacterial endosymbionts, such as Wolbachia and Spiroplasma species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts ag...

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Autores principales:	Juan C. Paredes, Jeremy K. Herren, Fanny Schüpfer, Bruno Lemaitre
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b9ea562da5f4c3a9ec0480178e82fbf
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spelling	oai:doaj.org-article:5b9ea562da5f4c3a9ec0480178e82fbf2021-11-15T15:50:18ZThe Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>10.1128/mBio.01006-162150-7511https://doaj.org/article/5b9ea562da5f4c3a9ec0480178e82fbf2016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01006-16https://doaj.org/toc/2150-7511ABSTRACT Insects commonly harbor facultative bacterial endosymbionts, such as Wolbachia and Spiroplasma species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts against natural enemies. While an increasing number of studies have reported endosymbiont-mediated protection, little is known about the mechanisms underlying this protection. Here, we analyze the mechanisms underlying protection from parasitoid wasps in Drosophila melanogaster mediated by its facultative endosymbiont Spiroplasma poulsonii. Our results indicate that S. poulsonii exerts protection against two distantly related wasp species, Leptopilina boulardi and Asobara tabida. S. poulsonii-mediated protection against parasitoid wasps takes place at the pupal stage and is not associated with an increased cellular immune response. In this work, we provide three important observations that support the notion that S. poulsonii bacteria and wasp larvae compete for host lipids and that this competition underlies symbiont-mediated protection. First, lipid quantification shows that both S. poulsonii and parasitoid wasps deplete D. melanogaster hemolymph lipids. Second, the depletion of hemolymphatic lipids using the Lpp RNA interference (Lpp RNAi) construct reduces wasp success in larvae that are not infected with S. poulsonii and blocks S. poulsonii growth. Third, we show that the growth of S. poulsonii bacteria is not affected by the presence of the wasps, indicating that when S. poulsonii is present, larval wasps will develop in a lipid-depleted environment. We propose that competition for host lipids may be relevant to endosymbiont-mediated protection in other systems and could explain the broad spectrum of protection provided. IMPORTANCE Virtually all insects, including crop pests and disease vectors, harbor facultative bacterial endosymbionts. They are vertically transmitted from mothers to their offspring, and some protect their host against pathogens. Here, we studied the mechanism of protection against parasitoid wasps mediated by the Drosophila melanogaster endosymbiont Spiroplasma poulsonii. Using genetic manipulation of the host, we provide strong evidence supporting the hypothesis that competition for host lipids underlies S. poulsonii-mediated protection against parasitoid wasps. We propose that lipid competition-based protection may not be restricted to Spiroplasma bacteria but could also apply other endosymbionts, notably Wolbachia bacteria, which can suppress human disease-causing viruses in insect hosts.Juan C. ParedesJeremy K. HerrenFanny SchüpferBruno LemaitreAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Juan C. Paredes Jeremy K. Herren Fanny Schüpfer Bruno Lemaitre The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>
description	ABSTRACT Insects commonly harbor facultative bacterial endosymbionts, such as Wolbachia and Spiroplasma species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts against natural enemies. While an increasing number of studies have reported endosymbiont-mediated protection, little is known about the mechanisms underlying this protection. Here, we analyze the mechanisms underlying protection from parasitoid wasps in Drosophila melanogaster mediated by its facultative endosymbiont Spiroplasma poulsonii. Our results indicate that S. poulsonii exerts protection against two distantly related wasp species, Leptopilina boulardi and Asobara tabida. S. poulsonii-mediated protection against parasitoid wasps takes place at the pupal stage and is not associated with an increased cellular immune response. In this work, we provide three important observations that support the notion that S. poulsonii bacteria and wasp larvae compete for host lipids and that this competition underlies symbiont-mediated protection. First, lipid quantification shows that both S. poulsonii and parasitoid wasps deplete D. melanogaster hemolymph lipids. Second, the depletion of hemolymphatic lipids using the Lpp RNA interference (Lpp RNAi) construct reduces wasp success in larvae that are not infected with S. poulsonii and blocks S. poulsonii growth. Third, we show that the growth of S. poulsonii bacteria is not affected by the presence of the wasps, indicating that when S. poulsonii is present, larval wasps will develop in a lipid-depleted environment. We propose that competition for host lipids may be relevant to endosymbiont-mediated protection in other systems and could explain the broad spectrum of protection provided. IMPORTANCE Virtually all insects, including crop pests and disease vectors, harbor facultative bacterial endosymbionts. They are vertically transmitted from mothers to their offspring, and some protect their host against pathogens. Here, we studied the mechanism of protection against parasitoid wasps mediated by the Drosophila melanogaster endosymbiont Spiroplasma poulsonii. Using genetic manipulation of the host, we provide strong evidence supporting the hypothesis that competition for host lipids underlies S. poulsonii-mediated protection against parasitoid wasps. We propose that lipid competition-based protection may not be restricted to Spiroplasma bacteria but could also apply other endosymbionts, notably Wolbachia bacteria, which can suppress human disease-causing viruses in insect hosts.
format	article
author	Juan C. Paredes Jeremy K. Herren Fanny Schüpfer Bruno Lemaitre
author_facet	Juan C. Paredes Jeremy K. Herren Fanny Schüpfer Bruno Lemaitre
author_sort	Juan C. Paredes
title	The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>
title_short	The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>
title_full	The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>
title_fullStr	The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>
title_full_unstemmed	The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>
title_sort	role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in <italic toggle="yes">drosophila</italic>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/5b9ea562da5f4c3a9ec0480178e82fbf
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The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in <italic toggle="yes">Drosophila</italic>

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