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Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

Commensal microbes in animals have a profound impact on tissue homeostasis, stress resistance, and ageing. We previously showed in Drosophila melanogaster that Acetobacter persici is a member of the gut microbiota that promotes ageing and shortens fly lifespan. However, the molecular mechanism by wh...

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Autores principales: Onuma, Taro, Yamauchi, Toshitaka, Kosakamoto, Hina, Kadoguchi, Hibiki, Kuraishi, Takayuki, Murakami, Takumi, Mori, Hiroshi, Miura, Masayuki, Obata, Fumiaki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112789/
https://www.ncbi.nlm.nih.gov/pubmed/37023169
http://dx.doi.org/10.1371/journal.pgen.1010709
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author Onuma, Taro
Yamauchi, Toshitaka
Kosakamoto, Hina
Kadoguchi, Hibiki
Kuraishi, Takayuki
Murakami, Takumi
Mori, Hiroshi
Miura, Masayuki
Obata, Fumiaki
author_facet Onuma, Taro
Yamauchi, Toshitaka
Kosakamoto, Hina
Kadoguchi, Hibiki
Kuraishi, Takayuki
Murakami, Takumi
Mori, Hiroshi
Miura, Masayuki
Obata, Fumiaki
author_sort Onuma, Taro
collection PubMed
description Commensal microbes in animals have a profound impact on tissue homeostasis, stress resistance, and ageing. We previously showed in Drosophila melanogaster that Acetobacter persici is a member of the gut microbiota that promotes ageing and shortens fly lifespan. However, the molecular mechanism by which this specific bacterial species changes lifespan and physiology remains unclear. The difficulty in studying longevity using gnotobiotic flies is the high risk of contamination during ageing. To overcome this technical challenge, we used a bacteria-conditioned diet enriched with bacterial products and cell wall components. Here, we demonstrate that an A. persici-conditioned diet shortens lifespan and increases intestinal stem cell (ISC) proliferation. Feeding adult flies a diet conditioned with A. persici, but not with Lactiplantibacillus plantarum, can decrease lifespan but increase resistance to paraquat or oral infection of Pseudomonas entomophila, indicating that the bacterium alters the trade-off between lifespan and host defence. A transcriptomic analysis using fly intestine revealed that A. persici preferably induces antimicrobial peptides (AMPs), while L. plantarum upregulates amidase peptidoglycan recognition proteins (PGRPs). The specific induction of these Imd target genes by peptidoglycans from two bacterial species is due to the stimulation of the receptor PGRP-LC in the anterior midgut for AMPs or PGRP-LE from the posterior midgut for amidase PGRPs. Heat-killed A. persici also shortens lifespan and increases ISC proliferation via PGRP-LC, but it is not sufficient to alter the stress resistance. Our study emphasizes the significance of peptidoglycan specificity in determining the gut bacterial impact on healthspan. It also unveils the postbiotic effect of specific gut bacterial species, which turns flies into a "live fast, die young" lifestyle.
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spelling pubmed-101127892023-04-19 Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan Onuma, Taro Yamauchi, Toshitaka Kosakamoto, Hina Kadoguchi, Hibiki Kuraishi, Takayuki Murakami, Takumi Mori, Hiroshi Miura, Masayuki Obata, Fumiaki PLoS Genet Research Article Commensal microbes in animals have a profound impact on tissue homeostasis, stress resistance, and ageing. We previously showed in Drosophila melanogaster that Acetobacter persici is a member of the gut microbiota that promotes ageing and shortens fly lifespan. However, the molecular mechanism by which this specific bacterial species changes lifespan and physiology remains unclear. The difficulty in studying longevity using gnotobiotic flies is the high risk of contamination during ageing. To overcome this technical challenge, we used a bacteria-conditioned diet enriched with bacterial products and cell wall components. Here, we demonstrate that an A. persici-conditioned diet shortens lifespan and increases intestinal stem cell (ISC) proliferation. Feeding adult flies a diet conditioned with A. persici, but not with Lactiplantibacillus plantarum, can decrease lifespan but increase resistance to paraquat or oral infection of Pseudomonas entomophila, indicating that the bacterium alters the trade-off between lifespan and host defence. A transcriptomic analysis using fly intestine revealed that A. persici preferably induces antimicrobial peptides (AMPs), while L. plantarum upregulates amidase peptidoglycan recognition proteins (PGRPs). The specific induction of these Imd target genes by peptidoglycans from two bacterial species is due to the stimulation of the receptor PGRP-LC in the anterior midgut for AMPs or PGRP-LE from the posterior midgut for amidase PGRPs. Heat-killed A. persici also shortens lifespan and increases ISC proliferation via PGRP-LC, but it is not sufficient to alter the stress resistance. Our study emphasizes the significance of peptidoglycan specificity in determining the gut bacterial impact on healthspan. It also unveils the postbiotic effect of specific gut bacterial species, which turns flies into a "live fast, die young" lifestyle. Public Library of Science 2023-04-06 /pmc/articles/PMC10112789/ /pubmed/37023169 http://dx.doi.org/10.1371/journal.pgen.1010709 Text en © 2023 Onuma et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Onuma, Taro
Yamauchi, Toshitaka
Kosakamoto, Hina
Kadoguchi, Hibiki
Kuraishi, Takayuki
Murakami, Takumi
Mori, Hiroshi
Miura, Masayuki
Obata, Fumiaki
Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan
title Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan
title_full Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan
title_fullStr Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan
title_full_unstemmed Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan
title_short Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan
title_sort recognition of commensal bacterial peptidoglycans defines drosophila gut homeostasis and lifespan
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112789/
https://www.ncbi.nlm.nih.gov/pubmed/37023169
http://dx.doi.org/10.1371/journal.pgen.1010709
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