Acute Sleep-Wake Cycle Shift Results in Community Alteration of Human Gut Microbiome

Abstract

Disturbances of sleep and the underlying circadian rhythm are related to many human diseases, such as obesity, diabetes, cardiovascular disorders, and cognitive impairments. Dysbiosis of the gut microbiome has also been reported to be associated with the pathologies of these diseases. Therefore, we proposed that disturbed sleep may regulate gut microbiota homeostasis. In this study, we mimicked the sleep-wake cycle shift, one typical type of circadian rhythm disturbances in young people, in recruited subjects. We used 16S rRNA gene amplicon sequencing to define microbial taxa from their fecal samples. Although the relative abundances of the microbes were not significantly altered, the functional-profile analysis of gut microbiota revealed functions enriched during the sleep-wake cycle shift. In addition, the microbial networks were quite distinct among baseline, shift, and recovery stages. These results suggest that an acute sleep-wake cycle shift may exert a limited influence on the gut microbiome, mainly including the functional profiles of the microbes and the microbial relationships within the microbial community. IMPORTANCE Circadian rhythm misalignment due to social jet lag, shift work, early morning starts, and delayed bedtimes is becoming common in our modern society. Disturbances of sleep and the underlying circadian rhythms are related to multiple human diseases, such as obesity, diabetes, cardiovascular disorders, and cognitive impairments. Given the crucial role of microbiota in the same pathologies as are caused by sleep disturbance, how the gut microbiota is affected by sleep is of increasing interest. The results of this study indicate that the acute circadian rhythm disturbance caused by sleep-wake shifts affect the human gut microbiota, especially the functional profiles of gut microbes and interactions among them. Further experiments with a longer-time-scale intervention and larger sample size are needed to assess the effects of chronic circadian rhythm disruption on the gut microbiome and to guide possible microbial therapies for clinical intervention in the related diseases.

Shiftwork, functional bowel symptoms, and the microbiome

“…For example, a study of 10 male security guards who worked both Full-size DOI: 10.7717/peerj.11406/fig- 5 day and night shifts found there were no significant differences in in alpha or beta diversity within and across-subject variation for both shifts (Mortas, Bilici & Karakan, 2020). In contrast, slight changes in microbial abundance and diversity were noted when 22 subjects, aged 20-35 years, delayed their sleep period for 2-4 h (Liu et al, 2020). Although there have been studies comparing circadian variation in the gut microbiota in mice (Thaiss et al, 2014) and another describing the results samples collected during multiple time points over several days by two subjects (Thaiss et al, 2014), our study is the first to compare the richness and diversity of gut microbiota collected from 51 human participants at two different time points in 24 h. Even though there are numerous studies that have reported increased and/or decreased amounts of various gut bacteria among patients with IBS (Bhattarai, Pedrogo & Kashyap, 2017;Casén et al, 2015;Pittayanon et al, 2019;Salonen, de Vos & Palva, 2010;Tap et al, 2017), a recent systematic review found only nine studies that discussed differences in alpha-diversity in patients with IBS compared to normal controls (Pittayanon et al, 2019).…”

“…For example, a study of 10 male security guards who worked both day and night shifts found there were no significant differences in in alpha or beta diversity within and across-subject variation for both shifts ( Mortas, Bilici & Karakan, 2020 ). In contrast, slight changes in microbial abundance and diversity were noted when 22 subjects, aged 20–35 years, delayed their sleep period for 2–4 h ( Liu et al, 2020 ). Although there have been studies comparing circadian variation in the gut microbiota in mice ( Thaiss et al, 2014 ) and another describing the results samples collected during multiple time points over several days by two subjects ( Thaiss et al, 2014 ), our study is the first to compare the richness and diversity of gut microbiota collected from 51 human participants at two different time points in 24 h.…”

Implication of Gut Microbiota in Cardiovascular Diseases

“…The interaction between circadian rhythms and diverse gut microbiota has been well studied, where the acute sleep-wake cycle shift alters the functional profiles of gut microbes. Together, the clock-microbial communities affect host homeostasis [ 58 ]. The circadian rhythm of SCFA production was observed by Segers et al to cause rhythmicity in intestinal movement [ 59 ].…”

Mammalian circadian systems: Organization and modern life challenges

“…Shift work promotes unhealthy snacking behaviour, as well as abnormal glucose tolerance, 182‐186 thereby increasing the risk for obesity and type 2 diabetes. In addition, circadian disruption because of genetic perturbation or misalignment of endogenous and exogenous rhythms has been found to cause dysbiosis of the gut microbiome 187‐190 . Vice versa, changes to the microbiome, for example by antibiotics, altered diet, age or stress, may disrupt endogenous clock functions of the gastrointestinal tract and promote metabolic disease 191 .…”