Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion

Abstract Mosquitoes rely on their microbiota for B vitamin synthesis. We previously found that Aedes aegypti third-instar larvae cleared of their microbiota were impaired in their development, notably due to a lack of folic acid (vitamin B9). In this study, we found that diet supplementation using a...

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Main Authors: Ottavia Romoli, Javier Serrato-Salas, Chloé Gapp, Yanouk Epelboin, Pol Figueras Ivern, Frédéric Barras, Mathilde Gendrin
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07319-7
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author Ottavia Romoli
Javier Serrato-Salas
Chloé Gapp
Yanouk Epelboin
Pol Figueras Ivern
Frédéric Barras
Mathilde Gendrin
author_facet Ottavia Romoli
Javier Serrato-Salas
Chloé Gapp
Yanouk Epelboin
Pol Figueras Ivern
Frédéric Barras
Mathilde Gendrin
author_sort Ottavia Romoli
collection DOAJ
description Abstract Mosquitoes rely on their microbiota for B vitamin synthesis. We previously found that Aedes aegypti third-instar larvae cleared of their microbiota were impaired in their development, notably due to a lack of folic acid (vitamin B9). In this study, we found that diet supplementation using a cocktail of seven B vitamins did not improve mosquito developmental success, but rather had a significant impact on the sex-ratio of the resulting adults, with an enrichment of female mosquitoes emerging from B vitamin-treated larvae. A transcriptomic analysis of male and female larvae identified some sex-specific regulated genes upon vitamin treatment. When treating germ-free larvae with individual B vitamins, we detected a specific toxic effect related to biotin (vitamin B7) exposure at high concentrations. We then provided germ-free larvae with varying biotin doses and showed that males are sensitive to biotin toxicity at a lower concentration than females. Gnotobiotic larvae exposed to controlled low bacterial counts or with bacteria characterised by slower growth, show a male-enriched adult population, suggesting that males require less bacteria-derived nutrients than females. These findings indicate that during larval development, mosquitoes have sex-specific nutritional requirements and toxicity thresholds, which impact the sex ratio of adults.
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spelling doaj-art-710be6c449654168b502d6eb0bfa53db2024-12-08T12:41:22ZengNature PortfolioCommunications Biology2399-36422024-12-017111010.1038/s42003-024-07319-7Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortionOttavia Romoli0Javier Serrato-Salas1Chloé Gapp2Yanouk Epelboin3Pol Figueras Ivern4Frédéric Barras5Mathilde Gendrin6Microbiota of Insect Vectors Group, Institut Pasteur de la GuyaneMicrobiota of Insect Vectors Group, Institut Pasteur de la GuyaneMicrobiota of Insect Vectors Group, Institut Pasteur de la GuyaneMicrobiota of Insect Vectors Group, Institut Pasteur de la GuyaneMicrobiota of Insect Vectors Group, Institut Pasteur de la GuyaneSAMe Unit, Department of Microbiology, Institut Pasteur, Université Paris Cité, CNRS UMR6047Microbiota of Insect Vectors Group, Institut Pasteur de la GuyaneAbstract Mosquitoes rely on their microbiota for B vitamin synthesis. We previously found that Aedes aegypti third-instar larvae cleared of their microbiota were impaired in their development, notably due to a lack of folic acid (vitamin B9). In this study, we found that diet supplementation using a cocktail of seven B vitamins did not improve mosquito developmental success, but rather had a significant impact on the sex-ratio of the resulting adults, with an enrichment of female mosquitoes emerging from B vitamin-treated larvae. A transcriptomic analysis of male and female larvae identified some sex-specific regulated genes upon vitamin treatment. When treating germ-free larvae with individual B vitamins, we detected a specific toxic effect related to biotin (vitamin B7) exposure at high concentrations. We then provided germ-free larvae with varying biotin doses and showed that males are sensitive to biotin toxicity at a lower concentration than females. Gnotobiotic larvae exposed to controlled low bacterial counts or with bacteria characterised by slower growth, show a male-enriched adult population, suggesting that males require less bacteria-derived nutrients than females. These findings indicate that during larval development, mosquitoes have sex-specific nutritional requirements and toxicity thresholds, which impact the sex ratio of adults.https://doi.org/10.1038/s42003-024-07319-7
spellingShingle Ottavia Romoli
Javier Serrato-Salas
Chloé Gapp
Yanouk Epelboin
Pol Figueras Ivern
Frédéric Barras
Mathilde Gendrin
Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion
Communications Biology
title Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion
title_full Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion
title_fullStr Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion
title_full_unstemmed Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion
title_short Nutritional sex-specificity on bacterial metabolites during mosquito (Aedes aegypti) development leads to adult sex-ratio distortion
title_sort nutritional sex specificity on bacterial metabolites during mosquito aedes aegypti development leads to adult sex ratio distortion
url https://doi.org/10.1038/s42003-024-07319-7
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