Ruminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis

Lixiang Zhai, Chunhua Huang, Ziwan Ning, Yijing Zhang, Min Zhuang, Wei Yang, Xiaolei Wang, Jingjing Wang, Lu Zhang, Haitao Xiao, Ling Zhao, Pallavi Asthana, Yan Y. Lam, Chi Fung Willis Chow, Jian-dong Huang, Shuofeng Yuan, Kui Ming Chan, Chun-Su Yuan, Johnson Yiu-Nam Lau, Hoi Leong Xavier Wong*Zhao-xiang Bian*

*Corresponding author for this work

Research output: Journal Publications and ReviewsRGC 21 - Publication in refereed journalpeer-review

118 Citations (Scopus)

Abstract

Diarrhea-predominant irritable bowel syndrome (IBS-D), a globally prevalent functional gastrointestinal (GI) disorder, is associated with elevated serotonin that increases gut motility. While anecdotal evidence suggests that the gut microbiota contributes to serotonin biosynthesis, mechanistic insights are limited. We determined that the bacterium Ruminococcus gnavus plays a pathogenic role in IBS-D. Monocolonization of germ-free mice with R. gnavus induced IBS-D-like symptoms, including increased GI transit and colonic secretion, by stimulating the production of peripheral serotonin. R. gnavus-mediated catabolism of dietary phenylalanine and tryptophan generated phenethylamine and tryptamine that directly stimulated serotonin biosynthesis in intestinal enterochromaffin cells via a mechanism involving activation of trace amine-associated receptor 1 (TAAR1). This R. gnavus-driven increase in serotonin levels elevated GI transit and colonic secretion but was abrogated upon TAAR1 inhibition. Collectively, our study provides molecular and pathogenetic insights into how gut microbial metabolites derived from dietary essential amino acids affect serotonin-dependent control of gut motility.
Original languageEnglish
Pages (from-to)33-44.e5
JournalCell Host and Microbe
Volume31
Issue number1
Online published9 Dec 2022
DOIs
Publication statusPublished - 11 Jan 2023

Funding

This work was kindly funded by the National Natural Science Foundation of China, China (82000504 to L.Z., 81973538 to Z.-X.B.); General Research Fund, Hong Kong (12102620 and 12102721 to Z.-X.B.); and Innovation and Technology Fund, Hong Kong (ITS/148/14FP to Z-X.B.). The authors thank the patients and healthy volunteers who participated in this study.

Research Keywords

  • aromatic trace amines
  • colonic secretion
  • gastrointestinal motility
  • gut microbiota
  • irritable bowel syndrome
  • phenethylamine
  • serotonin
  • trace amine-associated receptor 1
  • tryptamine

Fingerprint

Dive into the research topics of 'Ruminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis'. Together they form a unique fingerprint.

Cite this