Hallmarks of gut microbial rhythms
Gut microbial oscillations are widespread across studied species, having been identified in humans 34, meerkats26, mice 13, cows29,33, fish 31, and chickens30,32. Even host-associated microbiota of zooplankton undergo diurnal cycles 49. The proportion of gut members that show oscillating behaviour varies between studies and species, with between ~35% (humans) and ~80% (meerkats) of common taxa being identified as oscillators 12,26,34,50. This suggests natural variation in the strength of microbial oscillations across species. In industrialized societies of humans, population-wide gut microbial oscillations identified from cross-sectional studies appear to be weak34, and explain only a modest amount of variation in gut microbiota composition. In other species, circadian rhythms of the gut microbiota are strong and dominate over individual identity effects32 35 26,29.
Across the mammalian species studied thus far, there are some similarities in gut microbial dynamics across the day. In laboratory mice, the absolute abundance of bacteria inhabiting the mucosal epithelial layer peaks in the middle of the active phase11,13,40, with a 10-fold increase in bacterial numbers compared to the rest phase 11. This pattern is supported by increased number of bacteria in the gut more generally during the active phase 40. Similar findings were reported for wild meerkats, where reference standards were used to quantify 16S faecal abundance 26, and in humans, where the number of bacterial species in faecal samples peaks at midday34. Importantly, dissections of the mouse intestine show that faecal microbial rhythms reflect real changes to the composition of the intestinal microbiota 10,13, and are not simply a product of shedding patterns. Collectively, these findings also suggest that diurnal dynamics of gut microbes may be similar across host species.
Even though oscillating microbial taxa are likely to differ between host species, members of Clostridiales undergo some of the strongest and most consistent oscillations in mammals 7,11,35,39,40 and this may also be true for birds 30,32. There is also growing evidence from mice that different types of gut microbes peak at different times of the day. Some bacteria, termed here mucosal commensal s, colonise the mucosal gut lining, whilst others, termed hereluminal bacteria , are mostly found in the gut lumen. Mucosal commensals are hypothesized to have co-evolved with the host and form a protective layer against other bacteria between the gut epithelium and the gut lumen. In mice, mucosal commensals such as segmented filamentous bacteria (SFBs; order Clostridiales) peak at the start of the active phase and then commence to decline over the feeding period11,13. In contrast, many luminal bacteria have low abundances at the start of the active period yet increase after feeding11,13 (Fig. 1). Because the majority of taxa are luminal bacteria, these contrasting patterns result in increasing bacterial load over the active phase. However, the identification of oscillating taxa is biased by the fact that most studies apply relative rather than absolute abundances 40, which can generate misleading results, and by the difficulty of distinguishing between mucosal and luminal bacteria from metagenomic data.