Bei Li, Qianqian Yang, Min Li, Junqing He, Zhiqi Zhang, Xuchun Wan, Zihao Mo, Ruizhen Li, Shihan Li, Weirong Xu, Man Gu, Hanning Huang, Wei Li, Ziming Huang, Hongju Yang, Wei-Hua Chen, Zhi Liu
Autism spectrum disorder (ASD), a highly prevalent neurodevelopmental condition, is increasingly recognized for its strong association with the intestinal microbiome. However, the development of gut microbiota-targeted therapies has been impeded by a limited understanding of the molecular mechanisms underlying interactions between commensal bacteria and the host nervous system. In this study, shotgun metagenomic sequencing and UPLC-MS/MS targeted metabolic analyses identified altered tryptophan metabolites in the gut microbiota of both human ASD patients and ASD mouse models. Notably, we demonstrate that commensal bacteria-derived 5-hydroxytryptophan (5-HTP), metabolite of tryptophan, ameliorates anxiety, stereotypical and repetitive behaviors, as well as social deficits in these mouse models. Furthermore, 5-HTP is capable of crossing the blood-brain barrier and inhibits the overexpression of receptor tyrosine kinase (RTK) ligands, thereby suppressing the downstream RTK/MAPK/ERK signaling cascade. This inhibition subsequently normalizes the excessive stabilization of dendritic spines in the hippocampus in MeCP2 mouse. Our research demonstrates that gut microbiota producing 5-HTP improves ASD symptoms in various ASD animal models, elucidates the molecular mechanisms between gut microbiota and the onset and treatment of ASD, and provides a promising therapeutic approach for ameliorating ASD through the expression of neuron-regulated small molecules by gut indigenous bacteria.