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Response of the microbiome–gut–brain axis in Drosophila to amino acid deficit

Author

Listed:
  • Boram Kim

    (Seoul National University
    Korea Advanced Institute of Science and Technology)

  • Makoto I. Kanai

    (New York University Grossman School of Medicine)

  • Yangkyun Oh

    (New York University Grossman School of Medicine)

  • Minsoo Kyung

    (Seoul National University)

  • Eun-Kyoung Kim

    (Seoul National University)

  • In-Hwan Jang

    (Seoul National University)

  • Ji-Hoon Lee

    (Seoul National University)

  • Sang-Gyu Kim

    (Korea Advanced Institute of Science and Technology)

  • Greg S. B. Suh

    (Korea Advanced Institute of Science and Technology
    New York University Grossman School of Medicine
    KAIST Institute, Korea Advanced Institute of Science and Technology)

  • Won-Jae Lee

    (Seoul National University)

Abstract

A balanced intake of macronutrients—protein, carbohydrate and fat—is essential for the well-being of organisms. An adequate calorific intake but with insufficient protein consumption can lead to several ailments, including kwashiorkor1. Taste receptors (T1R1–T1R3)2 can detect amino acids in the environment, and cellular sensors (Gcn2 and Tor)3 monitor the levels of amino acids in the cell. When deprived of dietary protein, animals select a food source that contains a greater proportion of protein or essential amino acids (EAAs)4. This suggests that food selection is geared towards achieving the target amount of a particular macronutrient with assistance of the EAA-specific hunger-driven response, which is poorly understood. Here we show in Drosophila that a microbiome–gut–brain axis detects a deficit of EAAs and stimulates a compensatory appetite for EAAs. We found that the neuropeptide CNMamide (CNMa)5 was highly induced in enterocytes of the anterior midgut during protein deprivation. Silencing of the CNMa–CNMa receptor axis blocked the EAA-specific hunger-driven response in deprived flies. Furthermore, gnotobiotic flies bearing an EAA-producing symbiotic microbiome exhibited a reduced appetite for EAAs. By contrast, gnotobiotic flies with a mutant microbiome that did not produce leucine or other EAAs showed higher expression of CNMa and a greater compensatory appetite for EAAs. We propose that gut enterocytes sense the levels of diet- and microbiome-derived EAAs and communicate the EAA-deprived condition to the brain through CNMa.

Suggested Citation

  • Boram Kim & Makoto I. Kanai & Yangkyun Oh & Minsoo Kyung & Eun-Kyoung Kim & In-Hwan Jang & Ji-Hoon Lee & Sang-Gyu Kim & Greg S. B. Suh & Won-Jae Lee, 2021. "Response of the microbiome–gut–brain axis in Drosophila to amino acid deficit," Nature, Nature, vol. 593(7860), pages 570-574, May.
  • Handle: RePEc:nat:nature:v:593:y:2021:i:7860:d:10.1038_s41586-021-03522-2
    DOI: 10.1038/s41586-021-03522-2
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    Cited by:

    1. Yunpo Zhao & Mohammed A. Khallaf & Emilia Johansson & Najat Dzaki & Shreelatha Bhat & Johannes Alfredsson & Jianli Duan & Bill S. Hansson & Markus Knaden & Mattias Alenius, 2022. "Hedgehog-mediated gut-taste neuron axis controls sweet perception in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Junjun Gao & Song Zhang & Pan Deng & Zhigang Wu & Bruno Lemaitre & Zongzhao Zhai & Zheng Guo, 2024. "Dietary L-Glu sensing by enteroendocrine cells adjusts food intake via modulating gut PYY/NPF secretion," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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