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.