Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice

Abstract Gut microbiome is implicated in the onset and progression of major depressive disorder (MDD), but the dynamic alterations of depressive symptoms, gut microbiome, and fecal metabolome across different stages of stress exposure remain unclear. Here, we modified the chronic social defeat stres...

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Main Authors: Hongrui Li, Ping Liu, Tingfang Sun, Yifan Li, Jing Wu, Yu Huang, Jie Yang, Minghao Yuan, Jianping Zhang, Jian Yang, Ma-Li Wong, Julio Licinio, Peng Zheng
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-025-03326-2
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author Hongrui Li
Ping Liu
Tingfang Sun
Yifan Li
Jing Wu
Yu Huang
Jie Yang
Minghao Yuan
Jianping Zhang
Jian Yang
Ma-Li Wong
Julio Licinio
Peng Zheng
author_facet Hongrui Li
Ping Liu
Tingfang Sun
Yifan Li
Jing Wu
Yu Huang
Jie Yang
Minghao Yuan
Jianping Zhang
Jian Yang
Ma-Li Wong
Julio Licinio
Peng Zheng
author_sort Hongrui Li
collection DOAJ
description Abstract Gut microbiome is implicated in the onset and progression of major depressive disorder (MDD), but the dynamic alterations of depressive symptoms, gut microbiome, and fecal metabolome across different stages of stress exposure remain unclear. Here, we modified the chronic social defeat stress (CSDS) model to evaluate mice subjected to social defeat stress for 1, 4, 7, and 10 days. Behavioral tests, 16S rRNA, metagenomics, and fecal metabolomics were conducted to investigate the impact of stress exposure on behaviors, gut microbiota and fecal metabolites. We observed that depressive-like behaviors, such as anhedonia and social avoidance, worsened significantly as stress exposure increased. The microbial composition, function, and fecal metabolites exhibited distinct separations across the different social defeat stress groups. Mediation analysis identified key bacteria, such as Lachnospiraceae_UCG-001 and Bacteroidetes, and fecal metabolites like valeric acid and N-acetylaspartate. In our clinical depression cohort, we confirmed that fecal valeric acid levels, were significantly lower in depressive-like mice and MDD patients, correlating closely with stress exposure and anhedonia in mice. Further analysis of serum and brain metabolites in mice revealed sustained changes of N-acetylaspartate abundance in fecal, serum, and cortical samples following increasing stress exposure. Together, this study elucidated the characteristics of depressive-like behaviors, gut microbiome, and fecal metabolome across various social defeat stress exposure, and identified key bacteria and fecal metabolites potentially involved in modulating social defeat stress response and depressive-like behaviors, providing new insights into the pathogenesis and intervention of depression.
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spelling doaj-art-e9bd7e7d3e6c4db2b97acdef64b5b5642025-08-20T01:54:30ZengNature Publishing GroupTranslational Psychiatry2158-31882025-04-0115111210.1038/s41398-025-03326-2Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress miceHongrui Li0Ping Liu1Tingfang Sun2Yifan Li3Jing Wu4Yu Huang5Jie Yang6Minghao Yuan7Jianping Zhang8Jian Yang9Ma-Li Wong10Julio Licinio11Peng Zheng12Department of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityBeijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical UniversityDepartment of Psychiatry, College of Medicine, SUNY Upstate Medical UniversityDepartment of Psychiatry, College of Medicine, SUNY Upstate Medical UniversityDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical UniversityAbstract Gut microbiome is implicated in the onset and progression of major depressive disorder (MDD), but the dynamic alterations of depressive symptoms, gut microbiome, and fecal metabolome across different stages of stress exposure remain unclear. Here, we modified the chronic social defeat stress (CSDS) model to evaluate mice subjected to social defeat stress for 1, 4, 7, and 10 days. Behavioral tests, 16S rRNA, metagenomics, and fecal metabolomics were conducted to investigate the impact of stress exposure on behaviors, gut microbiota and fecal metabolites. We observed that depressive-like behaviors, such as anhedonia and social avoidance, worsened significantly as stress exposure increased. The microbial composition, function, and fecal metabolites exhibited distinct separations across the different social defeat stress groups. Mediation analysis identified key bacteria, such as Lachnospiraceae_UCG-001 and Bacteroidetes, and fecal metabolites like valeric acid and N-acetylaspartate. In our clinical depression cohort, we confirmed that fecal valeric acid levels, were significantly lower in depressive-like mice and MDD patients, correlating closely with stress exposure and anhedonia in mice. Further analysis of serum and brain metabolites in mice revealed sustained changes of N-acetylaspartate abundance in fecal, serum, and cortical samples following increasing stress exposure. Together, this study elucidated the characteristics of depressive-like behaviors, gut microbiome, and fecal metabolome across various social defeat stress exposure, and identified key bacteria and fecal metabolites potentially involved in modulating social defeat stress response and depressive-like behaviors, providing new insights into the pathogenesis and intervention of depression.https://doi.org/10.1038/s41398-025-03326-2
spellingShingle Hongrui Li
Ping Liu
Tingfang Sun
Yifan Li
Jing Wu
Yu Huang
Jie Yang
Minghao Yuan
Jianping Zhang
Jian Yang
Ma-Li Wong
Julio Licinio
Peng Zheng
Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice
Translational Psychiatry
title Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice
title_full Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice
title_fullStr Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice
title_full_unstemmed Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice
title_short Dynamic alterations of depressive-like behaviors, gut microbiome, and fecal metabolome in social defeat stress mice
title_sort dynamic alterations of depressive like behaviors gut microbiome and fecal metabolome in social defeat stress mice
url https://doi.org/10.1038/s41398-025-03326-2
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