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Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress

Eukaryotic genomes encode several buffering mechanisms that robustly maintain invariant phenotypic outcome despite fluctuating environmental conditions. Here we show that the Drosophila gut-associated commensals, represented by a single facultative symbiont, Lactobacillus plantarum (Lp(WJL)), consti...

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Autores principales: Ma, Dali, Bou-Sleiman, Maroun, Joncour, Pauline, Indelicato, Claire-Emmanuelle, Frochaux, Michael, Braman, Virginie, Litovchenko, Maria, Storelli, Gilles, Deplancke, Bart, Leulier, François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6704380/
https://www.ncbi.nlm.nih.gov/pubmed/31422284
http://dx.doi.org/10.1016/j.isci.2019.07.048
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author Ma, Dali
Bou-Sleiman, Maroun
Joncour, Pauline
Indelicato, Claire-Emmanuelle
Frochaux, Michael
Braman, Virginie
Litovchenko, Maria
Storelli, Gilles
Deplancke, Bart
Leulier, François
author_facet Ma, Dali
Bou-Sleiman, Maroun
Joncour, Pauline
Indelicato, Claire-Emmanuelle
Frochaux, Michael
Braman, Virginie
Litovchenko, Maria
Storelli, Gilles
Deplancke, Bart
Leulier, François
author_sort Ma, Dali
collection PubMed
description Eukaryotic genomes encode several buffering mechanisms that robustly maintain invariant phenotypic outcome despite fluctuating environmental conditions. Here we show that the Drosophila gut-associated commensals, represented by a single facultative symbiont, Lactobacillus plantarum (Lp(WJL)), constitutes a so far unexpected buffer that masks the contribution of the host's cryptic genetic variation (CGV) to developmental traits while the host is under nutritional stress. During chronic under-nutrition, Lp(WJL) consistently reduces variation in different host phenotypic traits and ensures robust organ patterning during development; Lp(WJL) also decreases genotype-dependent expression variation, particularly for development-associated genes. We further provide evidence that Lp(WJL) buffers via reactive oxygen species (ROS) signaling whose inhibition impairs microbiota-mediated phenotypic robustness. We thus identified a hitherto unappreciated contribution of the gut facultative symbionts to host fitness that, beyond supporting growth rates and maturation timing, confers developmental robustness and phenotypic homogeneity in times of nutritional stress.
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spelling pubmed-67043802019-08-26 Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress Ma, Dali Bou-Sleiman, Maroun Joncour, Pauline Indelicato, Claire-Emmanuelle Frochaux, Michael Braman, Virginie Litovchenko, Maria Storelli, Gilles Deplancke, Bart Leulier, François iScience Article Eukaryotic genomes encode several buffering mechanisms that robustly maintain invariant phenotypic outcome despite fluctuating environmental conditions. Here we show that the Drosophila gut-associated commensals, represented by a single facultative symbiont, Lactobacillus plantarum (Lp(WJL)), constitutes a so far unexpected buffer that masks the contribution of the host's cryptic genetic variation (CGV) to developmental traits while the host is under nutritional stress. During chronic under-nutrition, Lp(WJL) consistently reduces variation in different host phenotypic traits and ensures robust organ patterning during development; Lp(WJL) also decreases genotype-dependent expression variation, particularly for development-associated genes. We further provide evidence that Lp(WJL) buffers via reactive oxygen species (ROS) signaling whose inhibition impairs microbiota-mediated phenotypic robustness. We thus identified a hitherto unappreciated contribution of the gut facultative symbionts to host fitness that, beyond supporting growth rates and maturation timing, confers developmental robustness and phenotypic homogeneity in times of nutritional stress. Elsevier 2019-08-02 /pmc/articles/PMC6704380/ /pubmed/31422284 http://dx.doi.org/10.1016/j.isci.2019.07.048 Text en © 2019 The Author(s) http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Ma, Dali
Bou-Sleiman, Maroun
Joncour, Pauline
Indelicato, Claire-Emmanuelle
Frochaux, Michael
Braman, Virginie
Litovchenko, Maria
Storelli, Gilles
Deplancke, Bart
Leulier, François
Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress
title Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress
title_full Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress
title_fullStr Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress
title_full_unstemmed Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress
title_short Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress
title_sort commensal gut bacteria buffer the impact of host genetic variants on drosophila developmental traits under nutritional stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6704380/
https://www.ncbi.nlm.nih.gov/pubmed/31422284
http://dx.doi.org/10.1016/j.isci.2019.07.048
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