Larval microbiota primes the Drosophila adult gustatory response
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 pathoge...
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Nature Portfolio
2024-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-45532-4 |
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| author | Martina Montanari Gérard Manière Martine Berthelot-Grosjean Yves Dusabyinema Benjamin Gillet Yaël Grosjean C. Léopold Kurz Julien Royet |
| author_facet | Martina Montanari Gérard Manière Martine Berthelot-Grosjean Yves Dusabyinema Benjamin Gillet Yaël Grosjean C. Léopold Kurz Julien Royet |
| author_sort | Martina Montanari |
| collection | DOAJ |
| description | 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 germ-free 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. |
| format | Article |
| id | doaj-art-86b704e3010d4c40b6c989c13eb93fac |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-86b704e3010d4c40b6c989c13eb93fac2025-08-20T03:21:03ZengNature PortfolioNature Communications2041-17232024-02-0115111610.1038/s41467-024-45532-4Larval microbiota primes the Drosophila adult gustatory responseMartina Montanari0Gérard Manière1Martine Berthelot-Grosjean2Yves Dusabyinema3Benjamin Gillet4Yaël Grosjean5C. Léopold Kurz6Julien Royet7Aix-Marseille Université, CNRS, IBDMCentre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRAe, Université BourgogneCentre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRAe, Université BourgogneInstitut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de LyonInstitut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de LyonCentre des Sciences du Goût et de l’Alimentation, AgroSup Dijon, CNRS, INRAe, Université BourgogneAix-Marseille Université, CNRS, IBDMAix-Marseille Université, CNRS, IBDMAbstract 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 germ-free 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.https://doi.org/10.1038/s41467-024-45532-4 |
| spellingShingle | Martina Montanari Gérard Manière Martine Berthelot-Grosjean Yves Dusabyinema Benjamin Gillet Yaël Grosjean C. Léopold Kurz Julien Royet Larval microbiota primes the Drosophila adult gustatory response Nature Communications |
| title | Larval microbiota primes the Drosophila adult gustatory response |
| title_full | Larval microbiota primes the Drosophila adult gustatory response |
| title_fullStr | Larval microbiota primes the Drosophila adult gustatory response |
| title_full_unstemmed | Larval microbiota primes the Drosophila adult gustatory response |
| title_short | Larval microbiota primes the Drosophila adult gustatory response |
| title_sort | larval microbiota primes the drosophila adult gustatory response |
| url | https://doi.org/10.1038/s41467-024-45532-4 |
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