The Mouse Microbiome Is Required for Sex-Specific Diurnal Rhythms of Gene Expression and Metabolism

Weger, Benjamin D.; Gobet, Cédric; Yeung, Jake; Martin, Eva; Jimenez, Sonia; Betrisey, Bertrand; Foata, Francis; Berger, Bernard; Balvay, Aurélie; Foussier, Anne; Charpagne, Aline; Boizet-Bonhoure, Brigitte; Chou, Chieh Jason; Naef, Felix; Gachon, Frédéric

doi:10.1016/j.cmet.2018.09.023

Cited by 273Gut microbiota and healthCircadian rhythm and melatoninAnimal Nutrition and Physiology

The Mouse Microbiome Is Required for Sex-Specific Diurnal Rhythms of Gene Expression and Metabolism

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Weger, Benjamin D., Gobet, Cédric, Yeung, Jake, Martin, Eva, Jimenez, Sonia, Betrisey, Bertrand, Foata, Francis, Berger, Bernard +7 more·2019·Cell Metabolism

DOI 10.1016/j.cmet.2018.09.023PMC PMC6370974

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Abstract

The circadian clock and associated feeding rhythms have a profound impact on metabolism and the gut microbiome. To what extent microbiota reciprocally affect daily rhythms of physiology in the host remains elusive. Here, we analyzed transcriptome and metabolome profiles of male and female germ-free mice. While mRNA expression of circadian clock genes revealed subtle changes in liver, intestine, and white adipose tissue, germ-free mice showed considerably altered expression of genes associated with rhythmic physiology. Strikingly, the absence of the microbiome attenuated liver sexual dimorphism and sex-specific rhythmicity. The resulting feminization of male and masculinization of female germ-free animals is likely caused by altered sexual development and growth hormone secretion, associated with differential activation of xenobiotic receptors. This defines a novel mechanism by which the microbiome regulates host metabolism.

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Lacking exposure to microorganisms since birth, GF animals provide insights into how the microbiota is integral in shaping the behavior, physiology, and neurobiology of its host.
“Lacking exposure to microorganisms since birth, GF animals provide insights into how the microbiota is integral in shaping the behavior, physiology, and neurobiology of its host (Weger et al., 2019).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Weger et al., 2019
The Results section on rhythmic gene expression and metabolome (page not supplied) reports altered locomotor activity in germ-free female mice, supporting the behavioral part. The Introduction and Results also describe microbiota-related changes in metabolism, gene expression, and sexual maturation, supporting the physiological part. The paper does not establish the claim about host neurobiology, and its findings concern mice rather than GF animals generally. (LLM, conf=0.88)
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Impairment of Peripheral Circadian Clocks Precedes Metabolic Abnormalities in ob/ob Mice
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nhr-25, the Caenorhabditis elegans Ortholog of ftz-f1, Is Required for Epidermal and Somatic Gonad Development
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Genome-Wide Analysis of Chromatin States Reveals Distinct Mechanisms of Sex-Dependent Gene Regulation in Male and Female Mouse Liver
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Kieser S. Sarker S.A. Sakwinska O. Foata F. Sultana S. Khan Z. Islam S. Porta N. Combremont S. Betrisey B. Bangladeshi children with acute diarrhea show fecal microbiomes with increased Streptococcus abundance, irrespective of diarrhea etiology Environ. Microbiol. 2018 29786169

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Circadian rhythms in the gut microbiota shape sex differences in host gene expression and metabolismPreprint
Munyoki, S. K., Goff, J. P., Kolobaric, A., Long, A., Mullett, S. J., Burns, J. K., Jenkins, A. K., DePoy, L. M., Wendell, S. G., McClung, C. A., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.15.508006 · Cited by 3 · see citing works
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Authors: Weger, B. D., Gobet, C., Yeung, J., Martin, E., Jimenez, S., Betrisey, B., Foata, F., Berger, B., Balvay, A., Foussier, A., Charpagne, A., Boizet-Bonhoure, B., Chou, C. J., Naef, F., & Gachon, F.
Affiliations: Centre Hospitalier Universitaire Vaudois (CH)
École Polytechnique Fédérale de Lausanne (CH)
Nestlé (Switzerland) (CH)
AgroParisTech (FR)
Corresponding author: Gachon, Frédéric
ORCID: Weger, Benjamin D.
Gobet, Cédric
Yeung, Jake
Foata, Francis
Berger, Bernard
Balvay, Aurélie
Charpagne, Aline
Chou, Chieh Jason
Gachon, Frédéric
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2019-02
Volume: 29
Issue: 2
Pages: 362-382.e8
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2018.09.023
PMC: PMC6370974
OpenAlex: W2897926834
Cited by: 269
References: 193
Citations by year: 2026: 23 · 2025: 32 · 2024: 33 · 2023: 37 · 2022: 31 · 2021: 44 · 2020: 39 · 2019: 26 · 2018: 2 · 2017: 1
FWCI: 10.14
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Cell Metabolism (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
HAL (submittedVersion, cc-by-nc-nd)
Funders: European Research Council (ERC-2010-StG-260988)
Swiss National Science Foundation (310030_173079)
Natural Sciences and Engineering Research Council of Canada
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
Keywords: gut microbiota, circadian clock, sex differences, germ-free mice, growth hormone secretion, xenobiotic receptors, sexual development, metabolism, transcriptome, metabolome
MeSH terms: Gastrointestinal Microbiome, Animals, Circadian Rhythm, Female, Intestines, Liver, Male, Mice, Inbred C57BL, Sex Characteristics, Mice, Adipose Tissue, White, Ghrelin, Circadian Clocks, Transcriptome

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The Mouse Microbiome Is Required for Sex-Specific Diurnal Rhythms of Gene Expression and Metabolism

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