Dataset Information

Repeated sleep disruption in mice leads to persistent shifts in the fecal microbiome and metabolome.

ABSTRACT: It has been established in recent years that the gut microbiome plays a role in health and disease, potentially via alterations in metabolites that influence host physiology. Although sleep disruption and gut dysbiosis have been associated with many of the same diseases, studies investigating the gut microbiome in the context of sleep disruption have yielded inconsistent results, and have not assessed the fecal metabolome. We exposed mice to five days of sleep disruption followed by four days of ad libitum recovery sleep, and assessed the fecal microbiome and fecal metabolome at multiple timepoints using 16S rRNA gene amplicons and untargeted LC-MS/MS mass spectrometry. We found global shifts in both the microbiome and metabolome in the sleep-disrupted group on the second day of recovery sleep, when most sleep parameters had recovered to baseline levels. We observed an increase in the Firmicutes:Bacteroidetes ratio, along with decreases in the genus Lactobacillus, phylum Actinobacteria, and genus Bifidobacterium in sleep-disrupted mice compared to control mice. The latter two taxa remained low at the fourth day post-sleep disruption. We also identified multiple classes of fecal metabolites that were differentially abundant in sleep-disrupted mice, some of which are physiologically relevant and commonly influenced by the microbiome. This included bile acids, and inference of microbial functional gene content suggested reduced levels of the microbial bile salt hydrolase gene in sleep-disrupted mice. Overall, this study adds to the evidence base linking disrupted sleep to the gut microbiome and expands it to the fecal metabolome, identifying sleep disruption-sensitive bacterial taxa and classes of metabolites that may serve as therapeutic targets to improve health after poor sleep.

SUBMITTER: Bowers SJ

PROVIDER: S-EPMC7032712 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Repeated sleep disruption in mice leads to persistent shifts in the fecal microbiome and metabolome.

Bowers Samuel J SJ Vargas Fernando F González Antonio A He Shannon S Jiang Peng P Dorrestein Pieter C PC Knight Rob R Wright Kenneth P KP Lowry Christopher A CA Fleshner Monika M Vitaterna Martha H MH Turek Fred W FW

PloS one 20200220 2

It has been established in recent years that the gut microbiome plays a role in health and disease, potentially via alterations in metabolites that influence host physiology. Although sleep disruption and gut dysbiosis have been associated with many of the same diseases, studies investigating the gut microbiome in the context of sleep disruption have yielded inconsistent results, and have not assessed the fecal metabolome. We exposed mice to five days of sleep disruption followed by four days of ...[more]

PMID: 32078624

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Project description:BACKGROUNDThere has been a striking generational increase in the prevalence of food allergies. We have proposed that this increase can be explained, in part, by alterations in the commensal microbiome.METHODSTo identify bacterial signatures and metabolic pathways that may influence the expression of this disease, we collected fecal samples from a unique, well-controlled cohort of twins concordant or discordant for food allergy. Samples were analyzed by integrating 16S rRNA gene amplicon sequencing and liquid chromatography-tandem mass spectrometry metabolite profiling.RESULTSA bacterial signature of 64 operational taxonomic units (OTUs) distinguished healthy from allergic twins; the OTUs enriched in the healthy twins were largely taxa from the Clostridia class. We detected significant enrichment in distinct metabolite pathways in each group. The enrichment of diacylglycerol in healthy twins is of particular interest for its potential as a readily measurable fecal biomarker of health. In addition, an integrated microbial-metabolomic analysis identified a significant association between healthy twins and Phascolarctobacterium faecium and Ruminococcus bromii, suggesting new possibilities for the development of live microbiome-modulating biotherapeutics.CONCLUSIONTwin pairs exhibited significant differences in their fecal microbiomes and metabolomes through adulthood, suggesting that the gut microbiota may play a protective role in patients with food allergies beyond the infant stage.TRIAL REGISTRATIONParticipants in this study were recruited as part of an observational study (ClinicalTrials.gov NCT01613885) at multiple sites from 2014 to 2018.FUNDINGThis work was supported by the Sunshine Charitable Foundation; the Moss Family Foundation; the National Institute of Allergy and Infectious Diseases (NIAID) (R56AI134923 and R01AI 140134); the Sean N. Parker Center for Allergy and Asthma Research; the National Heart, Lung, and Blood Institute (R01 HL 118612); the Orsak family; the Kepner family; and the Stanford Institute for Immunity, Transplant and Infection.

Project description:The aim of this study was to explore the effects of saponins on the rumen microbiota and the ruminal metabolome. Alfalfa hay (AH) and soybean hulls (SH) were used as fiber sources for the control diets. The AH and SH diets were supplemented with tea saponins resulting in two additional diets named AHS and SHS, respectively. These 4 diets were fed to 24 young male Holstein cattle (n = 6 per diet). After 28 days of feeding, the rumen fluid from these cattle was collected using an oral stomach tube. Illumina MiSeq sequencing and ultrahigh-performance liquid chromatography coupled to quadrupole time-of-flight mass spectrometry (UHPLC-QTOF/MS) were used to investigate the changes in the ruminal microbes and their metabolites. The relative abundance of Prevotellaceae_YAB2003 increased, while Ruminococcaceae_NK4A214 and Lachnospiraceae_NK3A20 decreased in SHS and AHS compared to SH and AHS, respectively. Feeding SHS resulted in higher ruminal concentrations of squalene, lanosterol, 3-phenylpropanoic acid, and citrulline compared to SH. The different microbial genes predicted by Tax4Fun were involved in amino sugar and nucleotide sugar metabolism. The pathways of arginine and proline metabolism, purine metabolism, and pyrimidine metabolism were enriched by different metabolites. Moreover, in the SH group, a positive correlation was observed between Prevotella_1 (Bacteroidetes), Prevotellaceae_YAB2003 (Bacteroidetes), and Christensenellaceae_R.7 (Firmicutes), and the metabolites, including citrulline, lanosterol, and squalene. The increased abundances of Prevotella_1, Ruminococcaceae_UCG.002, and Prevotellaceae_YAB2003 might result in increased fiber digestion and nutrient utilization but nutrient digestion was not measured in the current study. In summary, saponins have the ability to modulate the ruminal microbial community and ruminal metabolites and thus affect the rumen environment. However, the response seems to be dependent on the composition of the basal diet. This study provides a comprehensive overview of the microbial and biochemical changes in the rumen of cattle fed saponins.

Dataset Information

Repeated sleep disruption in mice leads to persistent shifts in the fecal microbiome and metabolome.

Publications

Repeated sleep disruption in mice leads to persistent shifts in the fecal microbiome and metabolome.

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