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Mosquito‐bacteria interactions during larval development trigger metabolic changes with carry‐over effects on adult fitness

Authors :
Émilie Giraud
Hugo Varet
Rachel Legendre
Odile Sismeiro
Fabien Aubry
Stéphanie Dabo
Laura B. Dickson
Claire Valiente Moro
Louis Lambrechts
Interactions Virus-Insectes - Insect-Virus Interactions (IVI)
Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris]
Hub Bioinformatique et Biostatistique - Bioinformatics and Biostatistics HUB
Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)
Biomics (plateforme technologique)
Institut Pasteur [Paris]
Biologie des Bactéries pathogènes à Gram-positif - Biology of Gram-Positive Pathogens
The University of Texas Medical Branch (UTMB)
Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM)
Université Claude Bernard Lyon 1 (UCBL)
Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
This work was primarily funded by the Agence Nationale de la Recherche (grant ANR-16-CE35-0004-01). It was also supported by the French Government’s Investissement d’Avenir program Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases (grant ANR-10-LABX-62-IBEID to LL), and the City of Paris Emergence(s) program in Biomedical Research (to LL). The Biomics platform was supported by France Génomique (ANR-10-INBS-09-09) and IBISA.
ANR-16-CE35-0004,MOSQUIBIOTA,Contribution de la diversité bactérienne intestinale à la capacité vectorielle d'Aedes aegypti(2016)
ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010)
ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010)
Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Institut Pasteur [Paris] (IP)
Source :
Molecular Ecology, Molecular Ecology, Wiley, 2021, ⟨10.1111/mec.16327⟩, Molecular Ecology, 2022, 31 (5), pp.1444-1460. ⟨10.1111/mec.16327⟩
Publication Year :
2021
Publisher :
HAL CCSD, 2021.

Abstract

International audience; In animals with distinct life stages such as holometabolous insects, adult phenotypic variation is often shaped by the environment of immature stages, including their interactions with microbes colonizing larval habitats. Such carry-over effects were previously observed for several adult traits of the mosquito Aedes aegypti after larval exposure to different bacteria, but the mechanistic underpinnings are unknown. Here, we investigated the molecular changes triggered by gnotobiotic larval exposure to different bacteria in Ae. aegypti. We initially screened a panel of 16 bacterial isolates from natural mosquito breeding sites to determine their ability to influence adult life-history traits. We subsequently focused on four bacterial isolates (belonging to Flavobacterium, Lysobacter, Paenibacillus, and Enterobacteriaceae) with significant carry-over effects on adult survival and found that they were associated with distinct transcriptomic profiles throughout mosquito development. Moreover, we detected carry-over effects at the level of gene expression for the Flavobacterium and Paenibacillus isolates. The most prominent transcriptomic changes in gnotobiotic larvae reflected a profound remodeling of lipid metabolism, which translated into phenotypic differences in lipid storage and starvation resistance at the adult stage. Together, our findings indicate that larval exposure to environmental bacteria trigger substantial physiological changes that impact adult fitness, uncovering a possible mechanism underlying carry-over effects of mosquito-bacteria interactions during larval development.

Details

Language :
English
ISSN :
09621083 and 1365294X
Database :
OpenAIRE
Journal :
Molecular Ecology, Molecular Ecology, Wiley, 2021, ⟨10.1111/mec.16327⟩, Molecular Ecology, 2022, 31 (5), pp.1444-1460. ⟨10.1111/mec.16327⟩
Accession number :
edsair.doi.dedup.....8d458f52b255938c9b626a13689ccf6e
Full Text :
https://doi.org/10.1111/mec.16327⟩