Microbiome-emitted scents activate olfactory neuron-independent airway-gut-brain axis to promote host growth in Drosophila

Jin-Woo Lee, Kyung-Ah Lee, In-Hwan Jang, Kibum Nam, Sung-Hee Kim, Minsoo Kyung, Kyu-Chan Cho, Ji-hoon Lee, Hyejin You, Eun-Kyoung Kim, Young Hoon Koh, Hansol Lee, Junsun Park, Soo-Yeon Hwang, Youn Wook Chung, Choong-Min Ryu, Youngjoo Kwon, Soung-Hun Roh, Ji-Hwan Ryu and Won-Jae Lee ()
Additional contact information
Jin-Woo Lee: Seoul National University
Kyung-Ah Lee: Seoul National University
In-Hwan Jang: Seoul National University
Kibum Nam: Seoul National University
Sung-Hee Kim: Seoul National University
Minsoo Kyung: Seoul National University
Kyu-Chan Cho: Seoul National University
Ji-hoon Lee: Seoul National University
Hyejin You: Seoul National University
Eun-Kyoung Kim: Seoul National University
Young Hoon Koh: Seoul National University
Hansol Lee: Seoul National University
Junsun Park: Seoul National University
Soo-Yeon Hwang: Ewha Womans University
Youn Wook Chung: Yonsei University College of Medicine
Choong-Min Ryu: KRIBB
Youngjoo Kwon: Ewha Womans University
Soung-Hun Roh: Seoul National University
Ji-Hwan Ryu: Yonsei University College of Medicine
Won-Jae Lee: Seoul National University

Nature Communications, 2025, vol. 16, issue 1, 1-19

Abstract: Abstract While it is now accepted that the microbiome has strong impacts on animal growth promotion, the exact mechanism has remained elusive. Here we show that microbiome-emitted scents contain volatile somatotrophic factors (VSFs), which promote host growth in an olfaction-independent manner in Drosophila. We found that inhaled VSFs are readily sensed by olfactory receptor 42b non-neuronally expressed in subsets of tracheal airway cells, enteroendocrine cells, and enterocytes. Olfaction-independent sensing of VSFs activates the airway-gut-brain axis by regulating Hippo, FGF and insulin-like growth factor signaling pathways, which are required for airway branching, organ oxygenation and body growth. We found that a mutant microbiome that did not produce (2R,3R)-2,3-butanediol failed to activate the airway-gut-brain axis for host growth. Importantly, forced inhalation of (2R,3R)-2,3-butanediol completely reversed these defects. Our discovery of contact-independent and olfaction-independent airborne interactions between host and microbiome provides a novel perspective on the role of the airway-gut-brain axis in microbiome-controlled host development.

Date: 2025
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DOI: 10.1038/s41467-025-57484-4

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