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

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.

SUBMITTER: Weger BD

PROVIDER: S-EPMC6370974 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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

Weger Benjamin D BD Gobet Cédric C Yeung Jake J Martin Eva E Jimenez Sonia S Betrisey Bertrand B Foata Francis F Berger Bernard B Balvay Aurélie A Foussier Anne A Charpagne Aline A Boizet-Bonhoure Brigitte B Chou Chieh Jason CJ Naef Felix F Gachon Frédéric F

Cell metabolism 20181018 2

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 wi ...[more]

PMID: 30344015

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Project description:Obstructive sleep apnea (OSA), characterized by intermittent hypoxia and hypercapnia (IHC), affects the composition of the gut microbiome and metabolome. The gut microbiome has diurnal oscillations that play a crucial role in regulating circadian and overall metabolic homeostasis. Thus, we hypothesized that IHC adversely alters the gut luminal dynamics of key microbial families and metabolites. The objective of this study was to determine the diurnal dynamics of the fecal microbiome and metabolome of Apoe-/- mice after a week of IHC exposure. Individually housed, 10-week-old Apoe-/- mice on an atherogenic diet were split into two groups. One group was exposed to daily IHC conditions for 10 h (Zeitgeber time 2 [ZT2] to ZT12), while the other was maintained in room air. Six days after the initiation of the IHC conditions, fecal samples were collected every 4 h for 24 h (6 time points). We performed 16S rRNA gene amplicon sequencing and untargeted liquid chromatography-mass spectrometry (LC-MS) to assess changes in the microbiome and metabolome. IHC induced global changes in the cyclical dynamics of the gut microbiome and metabolome. Ruminococcaceae, Lachnospiraceae, S24-7, and Verrucomicrobiaceae had the greatest shifts in their diurnal oscillations. In the metabolome, bile acids, glycerolipids (phosphocholines and phosphoethanolamines), and acylcarnitines were greatly affected. Multi-omic analysis of these results demonstrated that Ruminococcaceae and tauro-β-muricholic acid (TβMCA) cooccur and are associated with IHC conditions and that Coriobacteriaceae and chenodeoxycholic acid (CDCA) cooccur and are associated with control conditions. IHC significantly change the diurnal dynamics of the fecal microbiome and metabolome, increasing members and metabolites that are proinflammatory and proatherogenic while decreasing protective ones. IMPORTANCE People with obstructive sleep apnea are at a higher risk of high blood pressure, type 2 diabetes, cardiac arrhythmias, stroke, and sudden cardiac death. We wanted to understand whether the gut microbiome changes induced by obstructive sleep apnea could potentially explain some of these medical problems. By collecting stool from a mouse model of this disease at multiple time points during the day, we studied how obstructive sleep apnea changed the day-night patterns of microbes and metabolites of the gut. Since the oscillations of the gut microbiome play a crucial role in regulating metabolism, changes in these oscillations can explain why these patients can develop so many metabolic problems. We found changes in microbial families and metabolites that regulate many metabolic pathways contributing to the increased risk for heart disease seen in patients with obstructive sleep apnea.

Dataset Information

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

Publications

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

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