Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue

Abstract The link between the gut microbiota and social behavior has been demonstrated, however the translational impact of a certain microbiota composition on stable behavioral patterns is yet to be elucidated. Here we employed an established social behavior mouse model of dominance (Dom) or submis...

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Autores principales: Oryan Agranyoni, Sapir Meninger-Mordechay, Atara Uzan, Oren Ziv, Mali Salmon-Divon, Dmitry Rodin, Olga Raz, Igor Koman, Omry Koren, Albert Pinhasov, Shiri Navon-Venezia
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Publicado: Nature Portfolio 2021
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Acceso en línea:https://doaj.org/article/11e347132a27466ab1f6683fe09abe20
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spelling oai:doaj.org-article:11e347132a27466ab1f6683fe09abe202021-12-02T16:31:03ZGut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue10.1038/s41522-021-00193-92055-5008https://doaj.org/article/11e347132a27466ab1f6683fe09abe202021-03-01T00:00:00Zhttps://doi.org/10.1038/s41522-021-00193-9https://doaj.org/toc/2055-5008Abstract The link between the gut microbiota and social behavior has been demonstrated, however the translational impact of a certain microbiota composition on stable behavioral patterns is yet to be elucidated. Here we employed an established social behavior mouse model of dominance (Dom) or submissiveness (Sub). A comprehensive 16S rRNA gene sequence analysis of Dom and Sub mice revealed a significantly different gut microbiota composition that clearly distinguishes between the two behavioral modes. Sub mice gut microbiota is significantly less diverse than that of Dom mice, and their taxa composition uniquely comprised the genera Mycoplasma and Anaeroplasma of the Tenericutes phylum, in addition to the Rikenellaceae and Clostridiaceae families. Conversely, the gut microbiota of Dom mice includes the genus Prevotella of the Bacteriodetes phylum, significantly less abundant in Sub mice. In addition, Sub mice show lower body weight from the age of 2 weeks and throughout their life span, accompanied with lower epididymis white adipose tissue (eWAT) mass and smaller adipocytes together with substantially elevated expression of inflammation and metabolic-related eWAT adipokines. Finally, fecal microbiota transplantation into germ-free mice show that Sub-transplanted mice acquired Sub microbiota and adopted their behavioral and physiological features, including depressive-like and anti-social behaviors alongside reduced eWAT mass, smaller adipocytes, and a Sub-like eWAT adipokine profile. Our findings demonstrate the critical role of the gut microbiome in determining dominance vs. submissiveness and suggest an association between gut microbiota, the eWAT metabolic and inflammatory profile, and the social behavior mode.Oryan AgranyoniSapir Meninger-MordechayAtara UzanOren ZivMali Salmon-DivonDmitry RodinOlga RazIgor KomanOmry KorenAlbert PinhasovShiri Navon-VeneziaNature PortfolioarticleMicrobial ecologyQR100-130ENnpj Biofilms and Microbiomes, Vol 7, Iss 1, Pp 1-14 (2021)
institution DOAJ
collection DOAJ
language EN
topic Microbial ecology
QR100-130
spellingShingle Microbial ecology
QR100-130
Oryan Agranyoni
Sapir Meninger-Mordechay
Atara Uzan
Oren Ziv
Mali Salmon-Divon
Dmitry Rodin
Olga Raz
Igor Koman
Omry Koren
Albert Pinhasov
Shiri Navon-Venezia
Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
description Abstract The link between the gut microbiota and social behavior has been demonstrated, however the translational impact of a certain microbiota composition on stable behavioral patterns is yet to be elucidated. Here we employed an established social behavior mouse model of dominance (Dom) or submissiveness (Sub). A comprehensive 16S rRNA gene sequence analysis of Dom and Sub mice revealed a significantly different gut microbiota composition that clearly distinguishes between the two behavioral modes. Sub mice gut microbiota is significantly less diverse than that of Dom mice, and their taxa composition uniquely comprised the genera Mycoplasma and Anaeroplasma of the Tenericutes phylum, in addition to the Rikenellaceae and Clostridiaceae families. Conversely, the gut microbiota of Dom mice includes the genus Prevotella of the Bacteriodetes phylum, significantly less abundant in Sub mice. In addition, Sub mice show lower body weight from the age of 2 weeks and throughout their life span, accompanied with lower epididymis white adipose tissue (eWAT) mass and smaller adipocytes together with substantially elevated expression of inflammation and metabolic-related eWAT adipokines. Finally, fecal microbiota transplantation into germ-free mice show that Sub-transplanted mice acquired Sub microbiota and adopted their behavioral and physiological features, including depressive-like and anti-social behaviors alongside reduced eWAT mass, smaller adipocytes, and a Sub-like eWAT adipokine profile. Our findings demonstrate the critical role of the gut microbiome in determining dominance vs. submissiveness and suggest an association between gut microbiota, the eWAT metabolic and inflammatory profile, and the social behavior mode.
format article
author Oryan Agranyoni
Sapir Meninger-Mordechay
Atara Uzan
Oren Ziv
Mali Salmon-Divon
Dmitry Rodin
Olga Raz
Igor Koman
Omry Koren
Albert Pinhasov
Shiri Navon-Venezia
author_facet Oryan Agranyoni
Sapir Meninger-Mordechay
Atara Uzan
Oren Ziv
Mali Salmon-Divon
Dmitry Rodin
Olga Raz
Igor Koman
Omry Koren
Albert Pinhasov
Shiri Navon-Venezia
author_sort Oryan Agranyoni
title Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
title_short Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
title_full Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
title_fullStr Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
title_full_unstemmed Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
title_sort gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/11e347132a27466ab1f6683fe09abe20
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