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Dietary prebiotics alter novel microbial dependent fecal metabolites that improve sleep.

ABSTRACT: Dietary prebiotics produce favorable changes in the commensal gut microbiome and reduce host vulnerability to stress-induced disruptions in complex behaviors such as sleep. The mechanisms for how prebiotics modulate stress physiology remain unclear; however, emerging evidence suggests that gut microbes and their metabolites may play a role. This study tested if stress and/or dietary prebiotics (Test diet) alter the fecal metabolome; and explored if these changes were related to sleep and/or gut microbial alpha diversity. Male F344 rats on either Test or Control diet were instrumented for electroencephalography biotelemetry measures of sleep/wake. After 5 weeks on diet, rats were either stressed or remained in home cages. Based on untargeted mass spectrometry and 16S rRNA gene sequencing, both stress and Test diet altered the fecal metabolome/microbiome. In addition, Test diet prevented the stress-induced reduction in microbial alpha diversity based on PD_Whole_Tree, which has been previously published. Network propagation analysis revealed that stress increased members of the neuroactive steroidal pregnane molecular family; and that Test diet reduced this effect. We also discovered links between sleep, alpha diversity, and pyrimidine, secondary bile acid, and neuroactive glucocorticoid/pregnanolone-type steroidal metabolites. These results reveal novel microbial-dependent metabolites that may modulate stress physiology and sleep.

SUBMITTER: Thompson RS

PROVIDER: S-EPMC7051969 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Dietary prebiotics alter novel microbial dependent fecal metabolites that improve sleep.

Thompson Robert S RS Vargas Fernando F Dorrestein Pieter C PC Chichlowski Maciej M Berg Brian M BM Fleshner Monika M

Scientific reports 20200302 1

Dietary prebiotics produce favorable changes in the commensal gut microbiome and reduce host vulnerability to stress-induced disruptions in complex behaviors such as sleep. The mechanisms for how prebiotics modulate stress physiology remain unclear; however, emerging evidence suggests that gut microbes and their metabolites may play a role. This study tested if stress and/or dietary prebiotics (Test diet) alter the fecal metabolome; and explored if these changes were related to sleep and/or gut ...[more]

PMID: 32123201

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Project description:BACKGROUND: High systemic estrogen levels contribute to breast cancer risk for postmenopausal women, whereas low levels contribute to osteoporosis risk. Except for obesity, determinants of non-ovarian systemic estrogen levels are undefined. We sought to identify members and functions of the intestinal microbial community associated with estrogen levels via enterohepatic recirculation. METHODS: Fifty-one epidemiologists at the National Institutes of Health, including 25 men, 7 postmenopausal women, and 19 premenopausal women, provided urine and aliquots of feces, using methods proven to yield accurate and reproducible results. Estradiol, estrone, 13 estrogen metabolites (EM), and their sum (total estrogens) were quantified in urine and feces by liquid chromatography/tandem mass spectrometry. In feces, ?-glucuronidase and ?-glucosidase activities were determined by realtime kinetics, and microbiome diversity and taxonomy were estimated by pyrosequencing 16S rRNA amplicons. Pearson correlations were computed for each loge estrogen level, loge enzymatic activity level, and microbiome alpha diversity estimate. For the 55 taxa with mean relative abundance of at least 0.1%, ordinal levels were created [zero, low (below median of detected sequences), high] and compared to loge estrogens, ?-glucuronidase and ?-glucosidase enzymatic activity levels by linear regression. Significance was based on two-sided tests with ?=0.05. RESULTS: In men and postmenopausal women, levels of total urinary estrogens (as well as most individual EM) were very strongly and directly associated with all measures of fecal microbiome richness and alpha diversity (R?0.50, P?0.003). These non-ovarian systemic estrogens also were strongly and significantly associated with fecal Clostridia taxa, including non-Clostridiales and three genera in the Ruminococcaceae family (R=0.57-0.70, P=0.03-0.002). Estrone, but not other EM, in urine correlated significantly with functional activity of fecal ?-glucuronidase (R=0.36, P=0.04). In contrast, fecal ?-glucuronidase correlated inversely with fecal total estrogens, both conjugated and deconjugated (R?-0.47, P?0.01). Premenopausal female estrogen levels, which were collected across menstrual cycles and thus highly variable, were completely unrelated to fecal microbiome and enzyme parameters (P?0.6). CONCLUSIONS: Intestinal microbial richness and functions, including but not limited to ?-glucuronidase, influence levels of non-ovarian estrogens via enterohepatic circulation. Thus, the gut microbial community likely affects the risk for estrogen-related conditions in older adults. Understanding how Clostridia taxa relate to systemic estrogens may identify targets for interventions.

Project description:It is well established that the gastrointestinal (GI) microbiota plays a major role in human health. Dietary interventions, and consumption of fermented foods that contain live microbes, in particular, are among the approaches being investigated to modulate the GI microbiota and improve health. However, the persistence of fermented food-associated bacteria (FAB) within the GI tract is typically limited by host factors that limit colonization and competition with autochthonous microbes. In this research, we examined if the addition of prebiotics, dietary substrates that are selectively metabolized by microbes to improve health, would enhance the persistence of FAB. We evaluated the persistence of bacteria from three live microbe-containing fermented foods-kefir, sausage, and sauerkraut-in fecal microbial communities from four healthy adults. Fecal communities were propagated in vitro and were inoculated with fermented food-associated microbes from kefir, sausage, or sauerkraut at ~107 CFU/mL. Communities were diluted 1:100 every 24 h into fresh gut simulation medium to simulate microbial community turnover in the GI tract. We measured the persistence of Lactobacillaceae from fermented foods by quantitative PCR (qPCR) and the persistence of other FAB through 16S rRNA gene sequencing. FAB were unable to persist in vitro, reaching undetectable levels within 96 h. Addition of prebiotics, including xylooligosaccharides and a mixture of fructooligosaccharides and galactooligosaccharides enhanced the persistence of some species of FAB, but the level of persistence varied by fecal donor, fermented food, and prebiotic tested. Addition of prebiotics also increased the relative abundance of Bifidobacterium species, which most likely originated from the fecal microbiota. Collectively, our results support previous in vivo studies demonstrating the transient nature of FAB in the GI tract and indicate that consumption of prebiotics may enhance their persistence.

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Dietary prebiotics alter novel microbial dependent fecal metabolites that improve sleep.

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Dietary prebiotics alter novel microbial dependent fecal metabolites that improve sleep.

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