External light‐dark cycle shapes gut microbiota through intrinsically photosensitive retinal ganglion cells

• Published in: EMBO reports Vol. 23; no. 6; pp. e52316 - n/a
• Main Authors: Lee, Chi‐Chan, Liang, Feng, Lee, I‐Chi, Lu, Tsung‐Hao, Shan, Yu‐Yau, Jeng, Chih‐Fan, Zou, Yan‐Fang, Yu, Hon‐Tsen, Chen (Alen), Shih‐Kuo
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 07-06-2022; Blackwell Publishing Ltd; John Wiley and Sons Inc
• Subjects: Abundance; Animal models; Animals; Biological clocks; Brain; Circadian Rhythm; Circadian rhythms; Circuits; Composition; Darkness; Digestive system; dim light at night; Dysbacteriosis; EMBO21; EMBO23; EMBO27; Gastrointestinal Microbiome; Gastrointestinal tract; Gene deletion; gut microbiota; High fat diet; Intestinal microflora; ipRGC; Light; Melanopsin; Metagenomics; Mice; Microbiota; Microorganisms; Nerves; Neurodegenerative diseases; Night; Nutrient deficiency; Oscillations; Photoperiod; Photosensitivity; Relative abundance; Retina; Retinal ganglion cells; Retinal Ganglion Cells - metabolism; RNA, Ribosomal, 16S - metabolism; Rod Opsins - genetics; Rod Opsins - metabolism; rRNA 16S; Sympathetic nerves; melanopsin; dim light at night; ipRGC; gut microbiota
• ISSN: 1469-221X; 1469-3178
• DOI: 10.15252/embr.202052316

Gut microbiota are involved in many physiological functions such as metabolism, brain development, and neurodegenerative diseases. Many microbes in the digestive tract do not maintain a constant level of their relative abundance but show daily oscillations under normal conditions. Recent evidence indicates that chronic jetlag, constant darkness, or deletion of the circadian core gene can alter the composition of gut microbiota and dampen the daily oscillation of gut microbes. However, the neuronal circuit responsible for modulating gut microbiota remained unclear. Using genetic mouse models and 16s rRNA metagenomic analysis, we find that light‐dark cycle information transmitted by the intrinsically photosensitive retinal ganglion cells (ipRGCs) is essential for daily oscillations of gut microbes under temporal restricted high‐fat diet conditions. Furthermore, aberrant light exposure such as dim light at night (dLAN) can alter the composition, relative abundance, and daily oscillations of gut microbiota. Together, our results indicate that external light‐dark cycle information can modulate gut microbiota in the direction from the brain to the gut via the sensory system.
Synopsis
In addition to the endogenous circadian clock of the host, the external light‐dark cycle can modulate gut microbiota composition, diversity, and daily oscillation through intrinsically photosensitive retinal ganglion cells.
Mice that lack intrinsically photosensitive retinal ganglion cells (ipRGCs) or melanopsin have a distinct gut microbiota composition from WT mice.
Light dark cycle information regulates the daily oscillation of gut microbiota through the ipRGC‐sympathetic nerve pathway.
Dim light at night causes dysbiosis through sympathetic nerve‐dependent and ‐independent pathways.
Graphical Abstract
In addition to the endogenous circadian clock of the host, the external light‐dark cycle can modulate gut microbiota composition, diversity, and daily oscillation through intrinsically photosensitive retinal ganglion cells.