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

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

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 in...

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Bibliographic Details
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
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Summary: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.
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content type line 23
ISSN:1469-221X
1469-3178
DOI:10.15252/embr.202052316