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Gut microbiota-derived butyrate primes systemic immunity in honeybees by mediating lipid metabolic reprogramming

ABSTRACT:

The gut microbiota plays a crucial role in insect immune priming, inducing memory-like response that functionally resembles adaptive immunity confined to vertebrates. While gut microbiota mediates systemic immune activation in insect hemolymph, the mechanisms underlying remote immunoregulation remain largely unknown. Using honeybee gut microbiota as a model, we identified butyrate as a key microbial metabolite coordinating immune-metabolic crosstalk. Butyrate supplementation restored immune competence in germ-free bees, mirroring the protective effects of microbiota-colonized individuals. Butyrate orchestrates lipid metabolic reprogramming in the fat body by activating glycerolipid and arachidonic acid metabolism through activating the G-protein coupled receptor 41 while inhibiting histone deacetylases. These changes in-turn upregulate prostaglandin E2 biosynthesis, which is essential for humoral and cellular immune activation. These findings unraveled that the intricate integration of immune and metabolic systems in honeybees is driven by gut-host interactions, a striking convergence found between these social insects and mammals.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive - reverse phase

PROVIDER: MTBLS13098 | MetaboLights | 2025-10-07

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS13098_LC-MS_negative_reverse-phase_metabolite_profiling.txt	Txt
	a_MTBLS13098_LC-MS_positive_reverse-phase_metabolite_profiling.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS13098_LC-MS_negative_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular
	m_MTBLS13098_LC-MS_positive_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular

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Project description:Background: Short-chain fatty acids (SCFAs), mainly acetate, propionate and butyrate, are produced by gut microbiota through fermentation of complex carbohydrates that cannot be digested by the human host. They affect gut health and can contribute at the distal level to the pathophysiology of several diseases, including renal pathologies. Methods: SCFA levels were measured in chronic kidney disease (CKD) patients (n = 54) at different stages of the disease and associations with renal function and inflammation parameters were examined. The impact of propionate and butyrate in pathways triggered in tubular cells under inflammatory conditions was analysed using genome-wide expression assays. Finally, a pre-clinical mouse model of folic acid-induced transition from acute kidney injury to CKD was used to analyse the preventive and therapeutic potential of these microbial metabolites in the development of CKD. Results: Faecal levels of propionate and butyrate in CKD patients gradually reduce as the disease progresses, and do so in close association with established clinical parameters for serum creatinine, blood urea nitrogen and the estimated glomerular filtration rate. Propionate and butyrate jointly downregulated the expression of 103 genes related to inflammatory processes and immune system activation triggered by TNF-α in tubular cells. In vivo, the administration of propionate and butyrate, either before or soon after injury, respectively prevented and slowed the progression of damage. This was indicated by a decrease in renal injury markers, the expression of pro-inflammatory and pro-fibrotic markers, and recovery of renal function over the long term. Conclusions: Propionate and butyrate levels are associated with a progressive loss of renal function in CKD patients. Early administration of these SCFAs prevents disease advancement in a pre-clinical model of acute renal damage, demonstrating their therapeutic potential independently of the gut microbiota.

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Gut microbiota-derived butyrate primes systemic immunity in honeybees by mediating lipid metabolic reprogramming

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