Diet and feeding pattern modulate diurnal dynamics of the ileal microbiome and transcriptome

Ana Carolina Dantas Machado; Steven D Brown; Amulya Lingaraju; Vignesh Sivaganesh; Cameron Martino; Amandine Chaix; Peng Zhao; Antonio F M Pinto; Max W Chang; R Alexander Richter; Alan Saghatelian; Alan R Saltiel; Rob Knight; Satchidananda Panda; Amir Zarrinpar

doi:10.1016/j.celrep.2022.111008

Diet and feeding pattern modulate diurnal dynamics of the ileal microbiome and transcriptome

Cell Rep. 2022 Jul 5;40(1):111008. doi: 10.1016/j.celrep.2022.111008.

Authors

Affiliations

¹ Division of Gastroenterology, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Department of Medicine, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA.
² Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA; Bioinformatics and Systems Biology Program, University of California, San Diego, La Jolla, CA, USA; Center for Microbiome Innovation, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA.
³ Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT, USA.
⁴ Department of Medicine, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Division of Metabolism and Endocrinology, Department of Medicine, University of California, San Diego, La Jolla, CA, USA.
⁵ Clayton Foundation Laboratories for Peptide Biology, the Salk Institute for Biological Studies, La Jolla, CA, USA.
⁶ Department of Medicine, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA.
⁷ Department of Medicine, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Division of Metabolism and Endocrinology, Department of Medicine, University of California, San Diego, La Jolla, CA, USA; Department of Pharmacology, Department of Medicine, University of California, San Diego, La Jolla, CA, USA; Institute of Diabetes and Metabolic Health, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA.
⁸ Department of Pediatrics, School of Medicine, University of California, San Diego, La Jolla, CA, USA; Center for Microbiome Innovation, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Department of Computer Science and Engineering, University of California, San Diego, La Jolla, CA, USA; Department of Bioengineering, University of California, San Diego, La Jolla, CA, USA.
⁹ Regulatory Biology Laboratory, The Salk Institute, 10010 N. Torrey Pines Road, La Jolla, CA, USA.
¹⁰ Division of Gastroenterology, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Department of Medicine, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Center for Microbiome Innovation, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; Institute of Diabetes and Metabolic Health, University of California, San Diego, 9500 Gilman Drive, MC 0983, La Jolla, CA, USA; VA Health Sciences, San Diego, La Jolla, CA, USA. Electronic address: azarrinpar@ucsd.edu.

Abstract

Compositional oscillations of the gut microbiome are essential for normal peripheral circadian rhythms, both of which are disrupted in diet-induced obesity (DIO). Although time-restricted feeding (TRF) maintains circadian synchrony and protects against DIO, its impact on the dynamics of the cecal gut microbiome is modest. Thus, other regions of the gut, particularly the ileum, the nexus for incretin and bile acid signaling, may play an important role in entraining peripheral circadian rhythms. We demonstrate the effect of diet and feeding rhythms on the ileal microbiome composition and transcriptome in mice. The dynamic rhythms of ileal microbiome composition and transcriptome are dampened in DIO. TRF partially restores diurnal rhythms of the ileal microbiome and transcriptome, increases GLP-1 release, and alters the ileal bile acid pool and farnesoid X receptor (FXR) signaling, which could explain how TRF exerts its metabolic benefits. Finally, we provide a web resource for exploration of ileal microbiome and transcriptome circadian data.

Keywords: 16S; CP: Microbiology; FXR; RNA-seq; bile acids; incretins; lumen; microbiota; small intestine.

Published by Elsevier Inc.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bile Acids and Salts
Diet
Feeding Behavior
Ileum / metabolism
Mice
Microbiota*
Obesity / metabolism
Transcriptome* / genetics

Substances

Bile Acids and Salts

Abstract

Publication types

MeSH terms

Substances

Grants and funding