Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment

Abstract Background Psychological health risk is one of the most severe and complex risks in manned deep-space exploration and long-term closed environments. Recently, with the in-depth research of the microbiota–gut–brain axis, gut microbiota has been considered a new approach to maintain and impro...

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Main Authors: Zikai Hao, Chen Meng, Leyuan Li, Siyuan Feng, Yinzhen Zhu, Jianlou Yang, Liangzhe Han, Leilei Sun, Weifeng Lv, Daniel Figeys, Hong Liu
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-023-01506-0
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author Zikai Hao
Chen Meng
Leyuan Li
Siyuan Feng
Yinzhen Zhu
Jianlou Yang
Liangzhe Han
Leilei Sun
Weifeng Lv
Daniel Figeys
Hong Liu
author_facet Zikai Hao
Chen Meng
Leyuan Li
Siyuan Feng
Yinzhen Zhu
Jianlou Yang
Liangzhe Han
Leilei Sun
Weifeng Lv
Daniel Figeys
Hong Liu
author_sort Zikai Hao
collection DOAJ
description Abstract Background Psychological health risk is one of the most severe and complex risks in manned deep-space exploration and long-term closed environments. Recently, with the in-depth research of the microbiota–gut–brain axis, gut microbiota has been considered a new approach to maintain and improve psychological health. However, the correlation between gut microbiota and psychological changes inside long-term closed environments is still poorly understood. Herein, we used the “Lunar Palace 365” mission, a 1-year-long isolation study in the Lunar Palace 1 (a closed manned Bioregenerative Life Support System facility with excellent performance), to investigate the correlation between gut microbiota and psychological changes, in order to find some new potential psychobiotics to maintain and improve the psychological health of crew members. Results We report some altered gut microbiota that were associated with psychological changes in the long-term closed environment. Four potential psychobiotics (Bacteroides uniformis, Roseburia inulinivorans, Eubacterium rectale, and Faecalibacterium prausnitzii) were identified. On the basis of metagenomic, metaproteomic, and metabolomic analyses, the four potential psychobiotics improved mood mainly through three pathways related to nervous system functions: first, by fermenting dietary fibers, they may produce short-chain fatty acids, such as butyric and propionic acids; second, they may regulate amino acid metabolism pathways of aspartic acid, glutamic acid, tryptophan, etc. (e.g., converting glutamic acid to gamma–aminobutyric acid; converting tryptophan to serotonin, kynurenic acid, or tryptamine); and third, they may regulate other pathways, such as taurine and cortisol metabolism. Furthermore, the results of animal experiments confirmed the positive regulatory effect and mechanism of these potential psychobiotics on mood. Conclusions These observations reveal that gut microbiota contributed to a robust effect on the maintenance and improvement of mental health in a long-term closed environment. Our findings represent a key step towards a better understanding the role of the gut microbiome in mammalian mental health during space flight and provide a basis for future efforts to develop microbiota-based countermeasures that mitigate risks to crew mental health during future long-term human space expeditions on the moon or Mars. This study also provides an essential reference for future applications of psychobiotics to neuropsychiatric treatments. Video Abstract
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spelling doaj.art-ea4ff79fd20b4bdfaf84d31aa4b202a92023-04-30T11:22:09ZengBMCMicrobiome2049-26182023-04-0111112210.1186/s40168-023-01506-0Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experimentZikai Hao0Chen Meng1Leyuan Li2Siyuan Feng3Yinzhen Zhu4Jianlou Yang5Liangzhe Han6Leilei Sun7Weifeng Lv8Daniel Figeys9Hong Liu10Institute of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang UniversityInstitute of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang UniversityDepartment of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaInstitute of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang UniversityInstitute of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang UniversityInstitute of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang UniversityState Key Laboratory of Software Development Environment, School of Computer Science and Engineering, Beihang UniversityState Key Laboratory of Software Development Environment, School of Computer Science and Engineering, Beihang UniversityState Key Laboratory of Software Development Environment, School of Computer Science and Engineering, Beihang UniversityDepartment of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaInstitute of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang UniversityAbstract Background Psychological health risk is one of the most severe and complex risks in manned deep-space exploration and long-term closed environments. Recently, with the in-depth research of the microbiota–gut–brain axis, gut microbiota has been considered a new approach to maintain and improve psychological health. However, the correlation between gut microbiota and psychological changes inside long-term closed environments is still poorly understood. Herein, we used the “Lunar Palace 365” mission, a 1-year-long isolation study in the Lunar Palace 1 (a closed manned Bioregenerative Life Support System facility with excellent performance), to investigate the correlation between gut microbiota and psychological changes, in order to find some new potential psychobiotics to maintain and improve the psychological health of crew members. Results We report some altered gut microbiota that were associated with psychological changes in the long-term closed environment. Four potential psychobiotics (Bacteroides uniformis, Roseburia inulinivorans, Eubacterium rectale, and Faecalibacterium prausnitzii) were identified. On the basis of metagenomic, metaproteomic, and metabolomic analyses, the four potential psychobiotics improved mood mainly through three pathways related to nervous system functions: first, by fermenting dietary fibers, they may produce short-chain fatty acids, such as butyric and propionic acids; second, they may regulate amino acid metabolism pathways of aspartic acid, glutamic acid, tryptophan, etc. (e.g., converting glutamic acid to gamma–aminobutyric acid; converting tryptophan to serotonin, kynurenic acid, or tryptamine); and third, they may regulate other pathways, such as taurine and cortisol metabolism. Furthermore, the results of animal experiments confirmed the positive regulatory effect and mechanism of these potential psychobiotics on mood. Conclusions These observations reveal that gut microbiota contributed to a robust effect on the maintenance and improvement of mental health in a long-term closed environment. Our findings represent a key step towards a better understanding the role of the gut microbiome in mammalian mental health during space flight and provide a basis for future efforts to develop microbiota-based countermeasures that mitigate risks to crew mental health during future long-term human space expeditions on the moon or Mars. This study also provides an essential reference for future applications of psychobiotics to neuropsychiatric treatments. Video Abstracthttps://doi.org/10.1186/s40168-023-01506-0Confined built environmentsLong-term closed environmentsGut microbiotaPsychobioticsMultiomicsMicrobiota–gut–brain axis
spellingShingle Zikai Hao
Chen Meng
Leyuan Li
Siyuan Feng
Yinzhen Zhu
Jianlou Yang
Liangzhe Han
Leilei Sun
Weifeng Lv
Daniel Figeys
Hong Liu
Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
Microbiome
Confined built environments
Long-term closed environments
Gut microbiota
Psychobiotics
Multiomics
Microbiota–gut–brain axis
title Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
title_full Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
title_fullStr Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
title_full_unstemmed Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
title_short Positive mood-related gut microbiota in a long-term closed environment: a multiomics study based on the “Lunar Palace 365” experiment
title_sort positive mood related gut microbiota in a long term closed environment a multiomics study based on the lunar palace 365 experiment
topic Confined built environments
Long-term closed environments
Gut microbiota
Psychobiotics
Multiomics
Microbiota–gut–brain axis
url https://doi.org/10.1186/s40168-023-01506-0
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