Gut Microbiota Orchestrates Energy Homeostasis during Cold

Claire Chevalier; Ozren Stojanović; Didier J. Colin; Nicolas Suarez-Zamorano; Valentina Tarallo; Christelle Veyrat-Durebex; Dorothée Rigo; Salvatore Fabbiano; Ana Stevanović; Stefanie Hagemann; Xavier Montet; Yann Seimbille; Nicola Zamboni; Siegfried Hapfelmeier; Mirko Trajkovski

doi:10.1016/j.cell.2015.11.004

Gut Microbiota Orchestrates Energy Homeostasis during Cold

Claire Chevalier, Ozren Stojanović, Didier J. Colin, Nicolas Suarez-Zamorano, Valentina Tarallo, Christelle Veyrat-Durebex, Dorothée Rigo, Salvatore Fabbiano, Ana Stevanović, Stefanie Hagemann, Xavier Montet, Yann Seimbille, Nicola Zamboni, Siegfried Hapfelmeier, Mirko Trajkovski^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

569 Citations (Scopus)

Abstract

Microbial functions in the host physiology are a result of the microbiota-host co-evolution. We show that cold exposure leads to marked shift of the microbiota composition, referred to as cold microbiota. Transplantation of the cold microbiota to germ-free mice is sufficient to increase insulin sensitivity of the host and enable tolerance to cold partly by promoting the white fat browning, leading to increased energy expenditure and fat loss. During prolonged cold, however, the body weight loss is attenuated, caused by adaptive mechanisms maximizing caloric uptake and increasing intestinal, villi, and microvilli lengths. This increased absorptive surface is transferable with the cold microbiota, leading to altered intestinal gene expression promoting tissue remodeling and suppression of apoptosis - the effect diminished by co-transplanting the most cold-downregulated strain Akkermansia muciniphila during the cold microbiota transfer. Our results demonstrate the microbiota as a key factor orchestrating the overall energy homeostasis during increased demand.

Original language	English
Pages (from-to)	1360-1374
Number of pages	15
Journal	Cell
Volume	163
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2015.11.004
Publication status	Published - 3 Dec 2015
Externally published	Yes

Bibliographical note

Funding Information:
We thank Maria Gustafsson Trajkovska, Claes Wollheim, and Roberto Coppari for discussions and critical reading; Jean-Baptiste Cavin and André Bado for sharing expertise in intestinal loop; Christian Darimont for help with bomb calorimetry; Abdessalam Cherkaoui and Jacques Schrenzel for the use of anaerobic incubator; (ERC-2013-StG-281904) to S.H. for partial support of the gnotobiotic research; Mirosava Ilievska for providing antibiotics; Mario Kreutzfeldt and Doron Merkler for help with histology quantifications; and Gabriel Waksman for support. The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013)/ERC grant agreement 336607 (ERC-2013-StG-336607); the Louis-Jeantet Foundation; Fondation pour Recherches Médicales; Novartis Foundation (14B053); and the Swiss National Science Foundation (SNSF) Professorship (PP00P3_144886) to M.T.

Publisher Copyright:
© 2015 Elsevier Inc. All rights reserved.

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10.1016/j.cell.2015.11.004

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@article{54acd8fe67164de8ac43e7781004a47a,

title = "Gut Microbiota Orchestrates Energy Homeostasis during Cold",

abstract = "Microbial functions in the host physiology are a result of the microbiota-host co-evolution. We show that cold exposure leads to marked shift of the microbiota composition, referred to as cold microbiota. Transplantation of the cold microbiota to germ-free mice is sufficient to increase insulin sensitivity of the host and enable tolerance to cold partly by promoting the white fat browning, leading to increased energy expenditure and fat loss. During prolonged cold, however, the body weight loss is attenuated, caused by adaptive mechanisms maximizing caloric uptake and increasing intestinal, villi, and microvilli lengths. This increased absorptive surface is transferable with the cold microbiota, leading to altered intestinal gene expression promoting tissue remodeling and suppression of apoptosis - the effect diminished by co-transplanting the most cold-downregulated strain Akkermansia muciniphila during the cold microbiota transfer. Our results demonstrate the microbiota as a key factor orchestrating the overall energy homeostasis during increased demand.",

author = "Claire Chevalier and Ozren Stojanovi{\'c} and Colin, {Didier J.} and Nicolas Suarez-Zamorano and Valentina Tarallo and Christelle Veyrat-Durebex and Doroth{\'e}e Rigo and Salvatore Fabbiano and Ana Stevanovi{\'c} and Stefanie Hagemann and Xavier Montet and Yann Seimbille and Nicola Zamboni and Siegfried Hapfelmeier and Mirko Trajkovski",

note = "Funding Information: We thank Maria Gustafsson Trajkovska, Claes Wollheim, and Roberto Coppari for discussions and critical reading; Jean-Baptiste Cavin and Andr{\'e} Bado for sharing expertise in intestinal loop; Christian Darimont for help with bomb calorimetry; Abdessalam Cherkaoui and Jacques Schrenzel for the use of anaerobic incubator; (ERC-2013-StG-281904) to S.H. for partial support of the gnotobiotic research; Mirosava Ilievska for providing antibiotics; Mario Kreutzfeldt and Doron Merkler for help with histology quantifications; and Gabriel Waksman for support. The research leading to these results has received funding from the European Research Council under the European Union{\textquoteright}s Seventh Framework Programme (FP/2007-2013)/ERC grant agreement 336607 (ERC-2013-StG-336607); the Louis-Jeantet Foundation; Fondation pour Recherches M{\'e}dicales; Novartis Foundation (14B053); and the Swiss National Science Foundation (SNSF) Professorship (PP00P3_144886) to M.T. Publisher Copyright: {\textcopyright} 2015 Elsevier Inc. All rights reserved.",

year = "2015",

month = dec,

day = "3",

doi = "10.1016/j.cell.2015.11.004",

language = "English",

volume = "163",

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AU - Stojanović, Ozren

AU - Colin, Didier J.

AU - Suarez-Zamorano, Nicolas

AU - Tarallo, Valentina

AU - Veyrat-Durebex, Christelle

AU - Rigo, Dorothée

AU - Fabbiano, Salvatore

AU - Stevanović, Ana

AU - Hagemann, Stefanie

AU - Montet, Xavier

AU - Seimbille, Yann

AU - Zamboni, Nicola

AU - Hapfelmeier, Siegfried

AU - Trajkovski, Mirko

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PY - 2015/12/3

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N2 - Microbial functions in the host physiology are a result of the microbiota-host co-evolution. We show that cold exposure leads to marked shift of the microbiota composition, referred to as cold microbiota. Transplantation of the cold microbiota to germ-free mice is sufficient to increase insulin sensitivity of the host and enable tolerance to cold partly by promoting the white fat browning, leading to increased energy expenditure and fat loss. During prolonged cold, however, the body weight loss is attenuated, caused by adaptive mechanisms maximizing caloric uptake and increasing intestinal, villi, and microvilli lengths. This increased absorptive surface is transferable with the cold microbiota, leading to altered intestinal gene expression promoting tissue remodeling and suppression of apoptosis - the effect diminished by co-transplanting the most cold-downregulated strain Akkermansia muciniphila during the cold microbiota transfer. Our results demonstrate the microbiota as a key factor orchestrating the overall energy homeostasis during increased demand.

AB - Microbial functions in the host physiology are a result of the microbiota-host co-evolution. We show that cold exposure leads to marked shift of the microbiota composition, referred to as cold microbiota. Transplantation of the cold microbiota to germ-free mice is sufficient to increase insulin sensitivity of the host and enable tolerance to cold partly by promoting the white fat browning, leading to increased energy expenditure and fat loss. During prolonged cold, however, the body weight loss is attenuated, caused by adaptive mechanisms maximizing caloric uptake and increasing intestinal, villi, and microvilli lengths. This increased absorptive surface is transferable with the cold microbiota, leading to altered intestinal gene expression promoting tissue remodeling and suppression of apoptosis - the effect diminished by co-transplanting the most cold-downregulated strain Akkermansia muciniphila during the cold microbiota transfer. Our results demonstrate the microbiota as a key factor orchestrating the overall energy homeostasis during increased demand.

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VL - 163

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JO - Cell

JF - Cell

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ER -

Gut Microbiota Orchestrates Energy Homeostasis during Cold

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