Gut microbiota alterations in response to sleep length among African-origin adults

Abstract

Sleep disorders are increasingly being characterized in modern society as contributing to a host of serious medical problems, including obesity and metabolic syndrome. Changes to the microbial community in the human gut have been reportedly associated with many of these cardiometabolic outcomes. In this study, we investigated the impact of sleep length on the gut microbiota in a large cohort of 655 participants of African descent, aged 25-45, from Ghana, South Africa (SA), Jamaica, and the United States (US). The sleep duration was self-reported via a questionnaire. Participants were classified into 3 sleep groups: short (<7hrs), normal (7-<9hrs), and long (≥9hrs). Forty-seven percent of US participants were classified as short sleepers and 88% of SA participants as long sleepers. Gut microbial composition analysis (16S rRNA gene sequencing) revealed that bacterial alpha diversity negatively correlated with sleep length (p<0.05). Furthermore, sleep length significantly contributed to the inter-individual beta diversity dissimilarity in gut microbial composition (p<0.01). Participants with both short and long-sleep durations exhibited significantly higher abundances of several taxonomic features, compared to normal sleep duration participants. The predicted relative proportion of two genes involved in the butyrate synthesis via lysine pathway were enriched in short sleep duration participants. Finally, co-occurrence relationships revealed by network analysis showed unique interactions among the short, normal and long duration sleepers. These results suggest that sleep length in humans may alter gut microbiota by driving population shifts of the whole microbiota and also specific changes in Exact Sequence Variants abundance, which may have implications for chronic inflammation associated diseases. The current findings suggest a possible relationship between disrupted sleep patterns and the composition of the gut microbiota. Prospective investigations in larger and more prolonged sleep researches and causally experimental studies are needed to confirm these findings, investigate the underlying mechanism and determine whether improving microbial homeostasis may buffer against sleep-related health decline in humans.

Fig 1. Sleep length can significantly impact intestinal microbiota community structure.

(A) Alpha diversity (Shannon index) between different sleep groups; * p < 0.05; *** p < 0.001. (B) Beta diversity analysis (weighted UniFrac distance) between different sleep groups; (C) Beta diversity analysis (unweighted UniFrac distance); and (D) Differential ESV abundance among short, normal and long sleepers, adjusted for BMI, age, gender and countries. ESVs with relative abundance ≥ 1% in at least one group shown. Data shown are means ± S.E.M.; * p(fdr-corrected) < 0.05. fdr, false discovery rate.

Fig 2. The network analysis revealing the co-occurrence patterns among short sleepers, normal sleepers and long sleepers.

A connection represents a strong (Spearman’s correlation coefficient ρ>0.6) and significant (P <0.05) correlation. A-C, co-occurrence network of short sleepers (A) normal sleepers (B) and long sleepers (C) The nodes represented unique ESV feature in the data sets. The size of each node is proportional to the relative abundance. Node color corresponds to phylum taxonomic classification. The edge thickness is equivalent to the correlation values. D-F, Topological features for each node in the network, (D) betweenness centralization, (E) closeness centrality and (F) node degree values. *** p< 0.0001.