Indole produced during dysbiosis mediates host-microorganism chemical communication

  1. Rui-Qiu Yang
  2. Yong-Hong Chen
  3. Qin-yi Wu
  4. Jie Tang
  5. Shan-Zhuang Niu
  6. Qiu Zhao
  7. Yi-Cheng Ma  Is a corresponding author
  8. Cheng-Gang Zou  Is a corresponding author
  1. Yunnan University, China
  2. Yunnan University of Traditional Chinese Medicine, China
  3. Chinese Academy of Medical Sciences and Peking Union Medical College, China

Abstract

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.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting source data file.

Article and author information

Author details

  1. Rui-Qiu Yang

    State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yong-Hong Chen

    State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Qin-yi Wu

    Yunnan Provincial Key Laboratory of Molecular Biology for Sinomedicine, Yunnan University of Traditional Chinese Medicine, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jie Tang

    Yunnan Key Laboratory of Vaccine Research Development on Severe Infectious Disease, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Shan-Zhuang Niu

    State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Qiu Zhao

    State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Yi-Cheng Ma

    State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China
    For correspondence
    mayc@ynu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  8. Cheng-Gang Zou

    State key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China
    For correspondence
    chgzou@ynu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5519-4402

Funding

Ministry of Science and Technology of the People's Republic of China (the National Key R&D Program of China, 2022YFD1400700)

  • Yi-Cheng Ma

Foundation for Innovative Research Groups of the National Natural Science Foundation of China (the National Natural Science Foundation of China,U1802233)

  • Cheng-Gang Zou

Yunnan Characteristic Plant Extraction Laboratory (Independent research fund,2022YKZY006)

  • Cheng-Gang Zou

Foundation for Innovative Research Groups of the National Natural Science Foundation of China (the National Natural Science Foundation of China,31900420)

  • Yi-Cheng Ma

Foundation for Innovative Research Groups of the National Natural Science Foundation of China (the National Natural Science Foundation of China,32260021)

  • Yi-Cheng Ma

Yunnan Province of China (he Major Science and Technology Project in Yunnan Province of China, 202001BC070004)

  • Cheng-Gang Zou

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Martin Sebastian Denzel, Altos Labs, United Kingdom

Version history

  1. Received: December 5, 2022
  2. Preprint posted: December 19, 2022 (view preprint)
  3. Accepted: November 3, 2023
  4. Accepted Manuscript published: November 21, 2023 (version 1)

Copyright

© 2023, Yang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Rui-Qiu Yang
  2. Yong-Hong Chen
  3. Qin-yi Wu
  4. Jie Tang
  5. Shan-Zhuang Niu
  6. Qiu Zhao
  7. Yi-Cheng Ma
  8. Cheng-Gang Zou
(2023)
Indole produced during dysbiosis mediates host-microorganism chemical communication
eLife 12:e85362.
https://doi.org/10.7554/eLife.85362

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