Humid heat environment causes anxiety-like disorder via impairing gut microbiota and bile acid metabolism in mice

Huandi Weng, Li Deng, Tianyuan Wang, Huachong Xu, Jialin Wu, Qinji Zhou, Lingtai Yu, Boli Chen, Li’an Huang, Yibo Qu, Libing Zhou () and Xiaoyin Chen ()
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Huandi Weng: The First Affiliated Hospital & Clinical Neuroscience Institute of Jinan University
Li Deng: Jinan University
Tianyuan Wang: Jinan University
Huachong Xu: Jinan University
Jialin Wu: Jinan University
Qinji Zhou: Jinan University
Lingtai Yu: Guangdong Key Laboratory of Non-human Primate Research
Boli Chen: Guangdong Key Laboratory of Non-human Primate Research
Li’an Huang: The First Affiliated Hospital & Clinical Neuroscience Institute of Jinan University
Yibo Qu: Guangdong Key Laboratory of Non-human Primate Research
Libing Zhou: The First Affiliated Hospital & Clinical Neuroscience Institute of Jinan University
Xiaoyin Chen: Jinan University

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract Climate and environmental changes threaten human mental health, but the impacts of specific environmental conditions on neuropsychiatric disorders remain largely unclear. Here, we show the impact of a humid heat environment on the brain and the gut microbiota using a conditioned housing male mouse model. We demonstrate that a humid heat environment can cause anxiety-like behaviour in male mice. Microbial 16 S rRNA sequencing analysis reveals that a humid heat environment caused gut microbiota dysbiosis (e.g., decreased abundance of Lactobacillus murinus), and metabolomics reveals an increase in serum levels of secondary bile acids (e.g., lithocholic acid). Moreover, increased neuroinflammation is indicated by the elevated expression of proinflammatory cytokines in the serum and cortex, activated PI3K/AKT/NF-κB signalling and a microglial response in the cortex. Strikingly, transplantation of the microbiota from mice reared in a humid heat environment readily recapitulates these abnormalities in germ-free mice, and these abnormalities are markedly reversed by Lactobacillus murinus administration. Human samples collected during the humid heat season also show a decrease in Lactobacillus murinus abundance and an increase in the serum lithocholic acid concentration. In conclusion, gut microbiota dysbiosis induced by a humid heat environment drives the progression of anxiety disorders by impairing bile acid metabolism and enhancing neuroinflammation, and probiotic administration is a potential therapeutic strategy for these disorders.

Date: 2024
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DOI: 10.1038/s41467-024-49972-w

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