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Larval microbiota primes the Drosophila adult gustatory response

Martina Montanari, Gérard Manière, Martine Berthelot-Grosjean, Yves Dusabyinema, Benjamin Gillet, Yaël Grosjean, C. Léopold Kurz, Julien Royet
doi: https://doi.org/10.1101/2023.03.14.532561
Martina Montanari
1Aix-Marseille Université, CNRS, IBDM, Marseille, France
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Gérard Manière
2Centre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRAe, Université Bourgogne Franche-Comté, F-21000 Dijon, France
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Martine Berthelot-Grosjean
2Centre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRAe, Université Bourgogne Franche-Comté, F-21000 Dijon, France
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Yves Dusabyinema
3Institut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de Lyon, CNRS UMR5242, F-69007 Lyon, France
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Benjamin Gillet
3Institut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de Lyon, CNRS UMR5242, F-69007 Lyon, France
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Yaël Grosjean
2Centre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRAe, Université Bourgogne Franche-Comté, F-21000 Dijon, France
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C. Léopold Kurz
1Aix-Marseille Université, CNRS, IBDM, Marseille, France
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  • For correspondence: leopold.kurz@univ-amu.fr julien.royet@univ-amu.fr
Julien Royet
1Aix-Marseille Université, CNRS, IBDM, Marseille, France
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  • For correspondence: leopold.kurz@univ-amu.fr julien.royet@univ-amu.fr
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Abstract

The survival of animals depends, among other things, on their ability to identify threats in their surrounding environment. Senses such as olfaction, vision and taste play an essential role in sampling their living environment, including microorganisms, some of which are potentially pathogenic. This study focuses on the mechanisms of detection of bacteria by the Drosophila gustatory system. We demonstrate that the peptidoglycan (PGN) that forms the cell wall of bacteria triggers an immediate feeding aversive response when detected by the gustatory system of adult flies. Although we identify ppk23+ and Gr66a+ gustatory neurons as necessary to transduce fly response to PGN, we demonstrate that they play very different roles in the process. Time-controlled functional inactivation and in vivo calcium imaging demonstrate that while ppk23+ neurons are required in the adult flies to directly transduce PGN signal, Gr66a+ neurons must be functional in larvae to allow future adults to become PGN sensitive. Furthermore, the ability of adult flies to respond to bacterial PGN is lost when they hatch from larvae reared under axenic conditions. Recolonization of axenic larvae, but not adults, with a single bacterial species, Lactobacillus brevis, is sufficient to restore the ability of adults to respond to PGN. Our data demonstrate that the genetic and environmental characteristics of the larvae are essential to make the future adults competent to respond to certain sensory stimuli such as PGN.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 14, 2023.
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Larval microbiota primes the Drosophila adult gustatory response
Martina Montanari, Gérard Manière, Martine Berthelot-Grosjean, Yves Dusabyinema, Benjamin Gillet, Yaël Grosjean, C. Léopold Kurz, Julien Royet
bioRxiv 2023.03.14.532561; doi: https://doi.org/10.1101/2023.03.14.532561
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Larval microbiota primes the Drosophila adult gustatory response
Martina Montanari, Gérard Manière, Martine Berthelot-Grosjean, Yves Dusabyinema, Benjamin Gillet, Yaël Grosjean, C. Léopold Kurz, Julien Royet
bioRxiv 2023.03.14.532561; doi: https://doi.org/10.1101/2023.03.14.532561

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