The microbiota coordinates diurnal rhythms in innate immunity with the circadian clock.

TitleThe microbiota coordinates diurnal rhythms in innate immunity with the circadian clock.
Publication TypeJournal Article
Year of Publication2021
AuthorsBrooks, JF, Behrendt, CL, Ruhn, KA, Lee, S, Raj, P, Takahashi, JS, Hooper, LV
JournalCell
Volume184
Issue16
Pagination4154-4167.e12
Date Published2021 08 05
ISSN1097-4172
KeywordsAnimals, Antimicrobial Cationic Peptides, Bacterial Adhesion, Cell Adhesion, Circadian Clocks, Circadian Rhythm, Epithelial Cells, Feeding Behavior, Gastrointestinal Microbiome, Immunity, Innate, Intestine, Small, Lymphocytes, Mice, Inbred C57BL, Muramidase, Pancreatitis-Associated Proteins, Salmonella Infections, Animal, Signal Transduction, STAT3 Transcription Factor
Abstract

<p>Environmental light cycles entrain circadian feeding behaviors in animals that produce rhythms in exposure to foodborne bacteria. Here, we show that the intestinal microbiota generates diurnal rhythms in innate immunity that synchronize with feeding rhythms to anticipate microbial exposure. Rhythmic expression of antimicrobial proteins was driven by daily rhythms in epithelial attachment by segmented filamentous bacteria (SFB), members of the mouse intestinal microbiota. Rhythmic SFB attachment was driven by the circadian clock through control of feeding rhythms. Mechanistically, rhythmic SFB attachment activated an immunological circuit involving group 3 innate lymphoid cells. This circuit triggered oscillations in epithelial STAT3 expression and activation that produced rhythmic antimicrobial protein expression and caused resistance to Salmonella Typhimurium infection to vary across the day-night cycle. Thus, host feeding rhythms synchronize with the microbiota to promote rhythms in intestinal innate immunity that anticipate exogenous microbial exposure.</p>

DOI10.1016/j.cell.2021.07.001
Alternate JournalCell
PubMed ID34324837
PubMed Central IDPMC8967342
Grant ListS10 OD020103 / OD / NIH HHS / United States
T32 AI005284 / AI / NIAID NIH HHS / United States
R01 DK070855 / DK / NIDDK NIH HHS / United States
/ HHMI / Howard Hughes Medical Institute / United States
R25 GM086262 / GM / NIGMS NIH HHS / United States