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other·preclinical research, biomedical research, immunology, gastroenterology·PMC10112789

Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

PLOS Genetics · 15 authors, 6 centres

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TL;DR

In Drosophila, a bacteria-conditioned diet enriched with peptidoglycans from Acetobacter persici, but not Lactiplantibacillus plantarum, shortens lifespan and increases intestinal stem cell proliferation. These effects are mediated through species-specific recognition of peptidoglycan structure by PGRP-LC and PGRP-LE receptors in distinct gut regions.

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This preclinical study used bacteria-conditioned diets (BacD) enriched with bacterial products and cell wall components to investigate how peptidoglycan (PGN) from two gut commensal species affects Drosophila physiology. A. persici-conditioned diet shortened lifespan and increased intestinal stem cell (ISC) proliferation, while L. plantarum-conditioned diet did not. Transcriptomic analysis of fly intestine showed that A. persici PGN induces antimicrobial peptides (AMPs) via PGRP-LC in the anterior midgut, whereas L. plantarum PGN upregulates amidase peptidoglycan recognition proteins (PGRPs) via PGRP-LE in the posterior midgut. Heat-killed A. persici also shortened lifespan and increased ISC proliferation through PGRP-LC, but was insufficient to alter stress resistance. The study suggests that structural differences in PGN between the two bacterial species are recognized by distinct PGRP receptors, and this specificity determines the impact on host healthspan, including a trade-off between lifespan and host defence.

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other

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preclinical research

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ORIGINAL PAPER

PMC10112789

Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan

PLOS Genetics

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ABSTRACT

Abstract 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.

CITATION EXPORT

Taro Onuma, Toshitaka Yamauchi, Hina Kosakamoto et al.. Recognition of commensal bacterial peptidoglycans defines Drosophila gut homeostasis and lifespan. PLOS Genetics. (2023). https://doi.org/10.1371/journal.pgen.1010709

AUTHORS

15 · 6 CENTRES

Taro Onuma, Toshitaka Yamauchi, Hina Kosakamoto, Hibiki Kadoguchi, Takayuki Kuraishi, Takumi Murakami, Hiroshi Mori, Masayuki Miura, Fumiaki Obata, Gregory P Copenhaver, Ville Hietakangas, Gregory P Copenhaver, Ville Hietakangas, Gregory P Copenhaver, Ville Hietakangas

1Department of Genetics, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan
2RIKEN Center for Biosystems Dynamics Research, Hyogo, Japan
3Faculty of Pharmacy, Institute of Medical, Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan
4Department of Informatics, National Institute of Genetics, Shizuoka, Japan
5Laboratory of Molecular Cell Biology and Development, Graduate School of Biostudies, Kyoto University, Kyoto, Japan
6University of Helsinki: Helsingin Yliopisto, FINLAND