Indole produced during dysbiosis mediates host–microorganism chemical communication

An imbalance of the gut microbiota, termed dysbiosis, has a substantial impact on host physiology. However, the mechanism by which host deals with gut dysbiosis to maintain fitness remains largely unknown. In Caenorhabditis elegans, Escherichia coli, which is its bacterial diet, proliferates in its...

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Main Authors: Rui-Qiu Yang, Yong-Hong Chen, Qin-yi Wu, Jie Tang, Shan-Zhuang Niu, Qiu Zhao, Yi-Cheng Ma, Cheng-Gang Zou
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/85362
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author Rui-Qiu Yang
Yong-Hong Chen
Qin-yi Wu
Jie Tang
Shan-Zhuang Niu
Qiu Zhao
Yi-Cheng Ma
Cheng-Gang Zou
author_facet Rui-Qiu Yang
Yong-Hong Chen
Qin-yi Wu
Jie Tang
Shan-Zhuang Niu
Qiu Zhao
Yi-Cheng Ma
Cheng-Gang Zou
author_sort Rui-Qiu Yang
collection DOAJ
description An imbalance of the gut microbiota, termed dysbiosis, has a substantial impact on host physiology. However, the mechanism by which host deals with gut dysbiosis to maintain fitness remains largely unknown. In Caenorhabditis elegans, Escherichia coli, which is its bacterial diet, proliferates in its intestinal lumen during aging. Here, we demonstrate that progressive intestinal proliferation of E. coli activates the transcription factor DAF-16, which is required for maintenance of longevity and organismal fitness in worms with age. DAF-16 up-regulates two lysozymes lys-7 and lys-8, thus limiting the bacterial accumulation in the gut of worms during aging. During dysbiosis, the levels of indole produced by E. coli are increased in worms. Indole is involved in the activation of DAF-16 by TRPA-1 in neurons of worms. Our finding demonstrates that indole functions as a microbial signal of gut dysbiosis to promote fitness of the host.
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spelling doaj.art-44e77e10611f4d059fb5bee44e43b96c2023-12-01T15:47:01ZengeLife Sciences Publications LtdeLife2050-084X2023-11-011210.7554/eLife.85362Indole produced during dysbiosis mediates host–microorganism chemical communicationRui-Qiu Yang0Yong-Hong Chen1Qin-yi Wu2Jie Tang3Shan-Zhuang Niu4Qiu Zhao5Yi-Cheng Ma6Cheng-Gang Zou7https://orcid.org/0000-0001-5519-4402State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, ChinaState key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, ChinaYunnan Provincial Key Laboratory of Molecular Biology for Sinomedicine, Yunnan University of Traditional Chinese Medicine, Kunming, ChinaState key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China; Yunnan Key Laboratory of Vaccine Research Development on Severe Infectious Disease, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, ChinaState key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, ChinaState key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, ChinaState key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, ChinaState key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, ChinaAn imbalance of the gut microbiota, termed dysbiosis, has a substantial impact on host physiology. However, the mechanism by which host deals with gut dysbiosis to maintain fitness remains largely unknown. In Caenorhabditis elegans, Escherichia coli, which is its bacterial diet, proliferates in its intestinal lumen during aging. Here, we demonstrate that progressive intestinal proliferation of E. coli activates the transcription factor DAF-16, which is required for maintenance of longevity and organismal fitness in worms with age. DAF-16 up-regulates two lysozymes lys-7 and lys-8, thus limiting the bacterial accumulation in the gut of worms during aging. During dysbiosis, the levels of indole produced by E. coli are increased in worms. Indole is involved in the activation of DAF-16 by TRPA-1 in neurons of worms. Our finding demonstrates that indole functions as a microbial signal of gut dysbiosis to promote fitness of the host.https://elifesciences.org/articles/85362C. elegansE. coliindoleDAF-16TRPA-1gut dysbiosis
spellingShingle Rui-Qiu Yang
Yong-Hong Chen
Qin-yi Wu
Jie Tang
Shan-Zhuang Niu
Qiu Zhao
Yi-Cheng Ma
Cheng-Gang Zou
Indole produced during dysbiosis mediates host–microorganism chemical communication
eLife
C. elegans
E. coli
indole
DAF-16
TRPA-1
gut dysbiosis
title Indole produced during dysbiosis mediates host–microorganism chemical communication
title_full Indole produced during dysbiosis mediates host–microorganism chemical communication
title_fullStr Indole produced during dysbiosis mediates host–microorganism chemical communication
title_full_unstemmed Indole produced during dysbiosis mediates host–microorganism chemical communication
title_short Indole produced during dysbiosis mediates host–microorganism chemical communication
title_sort indole produced during dysbiosis mediates host microorganism chemical communication
topic C. elegans
E. coli
indole
DAF-16
TRPA-1
gut dysbiosis
url https://elifesciences.org/articles/85362
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AT jietang indoleproducedduringdysbiosismediateshostmicroorganismchemicalcommunication
AT shanzhuangniu indoleproducedduringdysbiosismediateshostmicroorganismchemicalcommunication
AT qiuzhao indoleproducedduringdysbiosismediateshostmicroorganismchemicalcommunication
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AT chenggangzou indoleproducedduringdysbiosismediateshostmicroorganismchemicalcommunication