Intestinal GCN2 controls Drosophila systemic growth in response to Lactiplantibacillus plantarum symbiotic cues encoded by r/tRNA operons
- Ecole Normale Superieure de Lyon, CNRS UMR 5242, France
- University of Lyon, France
Abstract
Symbiotic bacteria interact with their host through symbiotic cues. Here, we took advantage of the mutualism between Drosophila and Lactiplantibacillus plantarum (Lp) to investigate a novel mechanism of host-symbiont interaction. Using chemically-defined diets, we found that association with Lp improves the growth of larvae fed amino acid-imbalanced diets, even though Lp cannot produce the limiting amino acid. We show that in this context Lp supports its host's growth through a molecular dialog that requires functional operons encoding ribosomal and transfer RNAs (r/tRNAs) in Lp and the GCN2 kinase in Drosophila's enterocytes. Our data indicate Lp's r/tRNAs are packaged in extracellular vesicles and activate GCN2 in a subset of larval enterocytes, a mechanism necessary to remodel the intestinal transcriptome and ultimately to support anabolic growth. Based on our findings, we propose a novel beneficial molecular dialog between host and microbes, which relies on a non-canonical role of GCN2 as a mediator of non-nutritional symbiotic cues encoded by r/tRNA operons.
Data availability
-RNAseq raw data are deposited at NCBI Sequence Read Archive under the numbers SUB10970982 and PRJNA799161.-Source data files containing all the numerical data used to generate the figures are provided for each figure.
Article and author information
Author details
Funding
Fondation pour la Recherche Médicale (DEQ20180339196)
- Théodore Grenier
- Jessika Consuegra
- Mariana G Ferrarini
- Houssam Akherraz
- Longwei Bai
- Yves Dusabyinema
- Isabelle Rahioui
- Pedro Da Silva
- Benjamin Gillet
- Sandrine Hughes
- Cathy I Ramos
- Renata C Matos
- François Leulier
Fondation pour la Recherche Médicale (SPF20170938612)
- Jessika Consuegra
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Sara Cherry, University of Pennsylvania, United States
Version history
- Preprint posted: October 31, 2021 (view preprint)
- Received: December 21, 2021
- Accepted: June 8, 2023
- Accepted Manuscript published: June 9, 2023 (version 1)
- Version of Record published: June 22, 2023 (version 2)
Copyright
© 2023, Grenier et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Intestinal GCN2 controls Drosophila systemic growth in response to Lactiplantibacillus plantarum symbiotic cues encoded by r/tRNA operons
eLife 12:e76584.
https://doi.org/10.7554/eLife.76584
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