TY - JOUR
T1 - Ruminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis
AU - Zhai, Lixiang
AU - Huang, Chunhua
AU - Ning, Ziwan
AU - Zhang, Yijing
AU - Zhuang, Min
AU - Yang, Wei
AU - Wang, Xiaolei
AU - Wang, Jingjing
AU - Zhang, Lu
AU - Xiao, Haitao
AU - Zhao, Ling
AU - Asthana, Pallavi
AU - Lam, Yan Y.
AU - Chow, Chi Fung Willis
AU - Huang, Jian-dong
AU - Yuan, Shuofeng
AU - Chan, Kui Ming
AU - Yuan, Chun-Su
AU - Lau, Johnson Yiu-Nam
AU - Wong, Hoi Leong Xavier
AU - Bian, Zhao-xiang
PY - 2023/1/11
Y1 - 2023/1/11
N2 - 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.
AB - 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.
KW - aromatic trace amines
KW - colonic secretion
KW - gastrointestinal motility
KW - gut microbiota
KW - irritable bowel syndrome
KW - phenethylamine
KW - serotonin
KW - trace amine-associated receptor 1
KW - tryptamine
UR - http://www.scopus.com/inward/record.url?scp=85146006778&partnerID=8YFLogxK
UR - https://www.scopus.com/record/pubmetrics.uri?eid=2-s2.0-85146006778&origin=recordpage
U2 - 10.1016/j.chom.2022.11.006
DO - 10.1016/j.chom.2022.11.006
M3 - RGC 21 - Publication in refereed journal
C2 - 36495868
SN - 1931-3128
VL - 31
SP - 33-44.e5
JO - Cell Host and Microbe
JF - Cell Host and Microbe
IS - 1
ER -