Microbiota-derived acetylcholine can promote gut motility in Drosophila melanogaster

Abstract

The gut microbiota is crucial for intestinal health, including gastrointestinal (GI) motility. How commensal bacterial species influence GI motility has not been fully elucidated. A major factor of GI motility is the gut contraction promoting the propulsive movement of orally ingested materials. Here, we developed a method to monitor and quantify gut contractions in living Drosophila melanogaster larvae. We found that the culture medium of an isolated strain Lactiplantibacillus plantarum Lsi promoted gut contraction in vivo , which was not observed in Leuconostoc sp. Leui nor Acetobacter persici Ai culture medium. To identify bacteria-derived metabolites, we performed metabolome analysis of the culture media by liquid chromatography-tandem mass spectrometry (LC–MS/MS). Of the 66 metabolites detected, we found that some metabolites changed in a species-specific manner. Among them, acetylcholine was specifically produced by L. plantarum. Feeding exogenous acetylcholine increased the frequency of gut contractions, which was blocked by D-tubocurarine, an inhibitor of nicotinic acetylcholine receptors. In this study, we propose a mechanism by which the gut microbiota influences Drosophila gut motility. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’.

Select Gut Bacteria Promote Mosquito Larval Growth by Contributing Protease Activity and Optimal Ionic Microenvironment for Protein Digestion

“…Pseudomonas, Serratia and Proteus ), frequently associated with mosquito microbiota (Scolari et a., 2019; Nafi et al, 1990). Notably, a recent study on another Dipteran larvae ( Drosophila ) has revealed an interesting mechanism of modulation of gastrointestinal contractions mediated through acetylcholine secreted by a gut associated bacterium, Lactiplantibacillus plantarum in a species-specific manner (Fujita et al, 2024), which reiterates a direct and species-specific role of gut associated bacteria in various aspects of larval physiology.…”

Lack of Single Amino Acids Transcriptionally Remodels Sensory Systems to Enhance the Intake of Protein and Microbiota

“…Beyond being a source of biomass themselves gut bacteria have been shown to reprogram animal physiology and behavior. They for example increase nutrient absorption and egg production in AA-deprived animals [54][55][56]61,63,112 . As such, they play an important role in helping animals to cope with AA deprivation states.…”

“…Recent work indicating that transcriptional dynamics play a crucial role in adapting sensory sensitivity in vertebrates suggests that transcriptional changes may have a greater impact on behavioral homeostasis across phyla than previously appreciated 52,53 . Under nutrient deprivation conditions, the gut microbiome has emerged as a crucial modulator of host physiology and behavior [54][55][56][57][58][59][60][61][62] . We have, for example, shown that in Drosophila, gut bacteria, including Lactobacilli, significantly impact feeding behavior and reproduction in eAA-deprived animals 3,56 .…”

Sculpting the microbiome

“…Fujita et al . [ 13 ] extend this discussion on the interplay of host and microbe physiology. In their study, they develop a new technique to allow visualization of gut peristalsis inside Drosophila, without sacrificing animals.…”