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.
Highlights
Dietary prebiotics produce favorable changes in the commensal gut microbiome and reduce host vulnerability to stress-induced disruptions in complex behaviors such as sleep
We previously reported that rats fed Test diet had an increase in non-rapid eye movement (NREM) sleep bout durations, when compared to those fed control diet [Fig. 4B,D from7]
Ingestion of a prebiotic diet (Test diet) improves undisturbed non-rapid eye movement (NREM) sleep, promotes REM sleep rebound after stress exposure, and prevents stress-induced reductions in gut microbial alpha diversity[7]
Summary
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 prebiotic diet-induced changes in the gut microbiota impact stress physiology remain unclear; there is emerging evidence that gut microbial metabolites likely play a role[12,13]. Bacterial dependent metabolites, such as short chain fatty acids and secondary bile acids, can signal the brain through the blood and/or vagal afferents[14,15,16]. Discovering and identifying gut metabolites that are modulated by diet and/or stress and relate to sleep and microbial alpha diversity adds to our understanding of microbiota-gut-brain signaling and could hasten the development of health promoting microbiome therapeutics. Based on this previous work, we hypothesize that prebiotic diet will alter the fecal metabolome and that these metabolomics changes will be related to our previously reported stress-protective effects of prebiotic diet on sleep and microbiome alpha diversity
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