Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex

Summary: Social dominance is a ubiquitous phenomenon among social animals, including humans. To date, individual attributes leading to dominance (after a contest) remain largely elusive. Here, we report that socially dominant rats can be distinguished from subordinates based on their intestinal micr...

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Main Authors: Tian Wang, Jinchun Xu, Yi Xu, Jie Xiao, Nanxi Bi, Xiaozhen Gu, Hui-Li Wang
Format: Article
Language:English
Published: Elsevier 2022-03-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S221112472200211X
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author Tian Wang
Jinchun Xu
Yi Xu
Jie Xiao
Nanxi Bi
Xiaozhen Gu
Hui-Li Wang
author_facet Tian Wang
Jinchun Xu
Yi Xu
Jie Xiao
Nanxi Bi
Xiaozhen Gu
Hui-Li Wang
author_sort Tian Wang
collection DOAJ
description Summary: Social dominance is a ubiquitous phenomenon among social animals, including humans. To date, individual attributes leading to dominance (after a contest) remain largely elusive. Here, we report that socially dominant rats can be distinguished from subordinates based on their intestinal microbiota. When dysbiosis is induced, rats are predisposed to a subordinate state, while dysbiotic rats reclaim social dominance following microbiota transplantation. Winning hosts are characterized by core microbes, a majority of which are associated with butyrate production, and the sole colonization of Clostridium butyricum is sufficient to restore dominance. Regarding molecular aspects, a histone deacetylase, HDAC2, is responsive to microbial status and mediates competition outcome; however, this occurs only in a restricted population of cells in the medial prefrontal cortex (mPFC). Furthermore, HDAC2 acts by modulating synaptic activity in mPFC. Together, these findings uncover a link between commensals and host dominance, providing insight into the gut-brain mechanisms underlying dominance determination.
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spelling doaj.art-41dc331dda704bb69a90822e4e3ae5ab2022-12-21T16:43:11ZengElsevierCell Reports2211-12472022-03-013810110478Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortexTian Wang0Jinchun Xu1Yi Xu2Jie Xiao3Nanxi Bi4Xiaozhen Gu5Hui-Li Wang6School of Food and Bioengineering, Hefei University of Technology, Hefei 230009, ChinaSchool of Food and Bioengineering, Hefei University of Technology, Hefei 230009, ChinaSchool of Food and Bioengineering, Hefei University of Technology, Hefei 230009, China; Engineering Research Center of Bio-process, Ministry of Education, Hefei University of Technology, 193 Tunxi Road, Hefei 230009, China; Corresponding authorSchool of Food and Bioengineering, Hefei University of Technology, Hefei 230009, ChinaSchool of Food and Bioengineering, Hefei University of Technology, Hefei 230009, ChinaSchool of Food and Bioengineering, Hefei University of Technology, Hefei 230009, ChinaSchool of Food and Bioengineering, Hefei University of Technology, Hefei 230009, China; Engineering Research Center of Bio-process, Ministry of Education, Hefei University of Technology, 193 Tunxi Road, Hefei 230009, China; Corresponding authorSummary: Social dominance is a ubiquitous phenomenon among social animals, including humans. To date, individual attributes leading to dominance (after a contest) remain largely elusive. Here, we report that socially dominant rats can be distinguished from subordinates based on their intestinal microbiota. When dysbiosis is induced, rats are predisposed to a subordinate state, while dysbiotic rats reclaim social dominance following microbiota transplantation. Winning hosts are characterized by core microbes, a majority of which are associated with butyrate production, and the sole colonization of Clostridium butyricum is sufficient to restore dominance. Regarding molecular aspects, a histone deacetylase, HDAC2, is responsive to microbial status and mediates competition outcome; however, this occurs only in a restricted population of cells in the medial prefrontal cortex (mPFC). Furthermore, HDAC2 acts by modulating synaptic activity in mPFC. Together, these findings uncover a link between commensals and host dominance, providing insight into the gut-brain mechanisms underlying dominance determination.http://www.sciencedirect.com/science/article/pii/S221112472200211Xsocial dominancegut microbiotaHDAC2sodium butyratemedial prefrontal cortex
spellingShingle Tian Wang
Jinchun Xu
Yi Xu
Jie Xiao
Nanxi Bi
Xiaozhen Gu
Hui-Li Wang
Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex
Cell Reports
social dominance
gut microbiota
HDAC2
sodium butyrate
medial prefrontal cortex
title Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex
title_full Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex
title_fullStr Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex
title_full_unstemmed Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex
title_short Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex
title_sort gut microbiota shapes social dominance through modulating hdac2 in the medial prefrontal cortex
topic social dominance
gut microbiota
HDAC2
sodium butyrate
medial prefrontal cortex
url http://www.sciencedirect.com/science/article/pii/S221112472200211X
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