Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude

Abstract Background Gut microbiota is significantly influenced by altitude. However, the dynamics of gut microbiota in relation to altitude remains undisclosed. Methods In this study, we investigated the microbiome profile of 610 healthy young men from three different places in China, grouped by alt...

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Main Authors: Yang Han, Xiaoshuang Liu, Qian Jia, Jiayu Xu, Jinlong Shi, Xiang Li, Guotong Xie, Xiaojing Zhao, Kunlun He
Format: Article
Language:English
Published: BMC 2024-04-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-024-01781-5
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author Yang Han
Xiaoshuang Liu
Qian Jia
Jiayu Xu
Jinlong Shi
Xiang Li
Guotong Xie
Xiaojing Zhao
Kunlun He
author_facet Yang Han
Xiaoshuang Liu
Qian Jia
Jiayu Xu
Jinlong Shi
Xiang Li
Guotong Xie
Xiaojing Zhao
Kunlun He
author_sort Yang Han
collection DOAJ
description Abstract Background Gut microbiota is significantly influenced by altitude. However, the dynamics of gut microbiota in relation to altitude remains undisclosed. Methods In this study, we investigated the microbiome profile of 610 healthy young men from three different places in China, grouped by altitude, duration of residence, and ethnicity. We conducted widely targeted metabolomic profiling and clinical testing to explore metabolic characteristics. Results Our findings revealed that as the Han individuals migrated from low altitude to high latitude, the gut microbiota gradually converged towards that of the Tibetan populations but reversed upon returning to lower altitude. Across different cohorts, we identified 51 species specifically enriched during acclimatization and 57 species enriched during deacclimatization to high altitude. Notably, Prevotella copri was found to be the most enriched taxon in both Tibetan and Han populations after ascending to high altitude. Furthermore, significant variations in host plasma metabolome and clinical indices at high altitude could be largely explained by changes in gut microbiota composition. Similar to Tibetans, 41 plasma metabolites, such as lactic acid, sphingosine-1-phosphate, taurine, and inositol, were significantly elevated in Han populations after ascending to high altitude. Germ-free animal experiments demonstrated that certain species, such as Escherichia coli and Klebsiella pneumoniae, which exhibited altitude-dependent variations in human populations, might play crucial roles in host purine metabolism. Conclusions This study provides insights into the dynamics of gut microbiota and host plasma metabolome with respect to altitude changes, indicating that their dynamics may have implications for host health at high altitude and contribute to host adaptation. Video Abstract
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spelling doaj.art-ff08332bdce34971ac1555d2478553c42024-04-07T11:24:52ZengBMCMicrobiome2049-26182024-04-0112112210.1186/s40168-024-01781-5Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitudeYang Han0Xiaoshuang Liu1Qian Jia2Jiayu Xu3Jinlong Shi4Xiang Li5Guotong Xie6Xiaojing Zhao7Kunlun He8 Medical Big Data Research Center, Medical Innovation Research Division, Chinese PLA General HospitalPing An Healthcare Technology Beijing Key Laboratory of Precision Medicine for Chronic Heart Failure, Medical Innovation Research Division, Chinese PLA General Hospital Medical Big Data Research Center, Medical Innovation Research Division, Chinese PLA General Hospital Medical Big Data Research Center, Medical Innovation Research Division, Chinese PLA General HospitalPing An Healthcare TechnologyPing An Healthcare Technology, Ping An Health Cloud Company Limited Beijing Key Laboratory of Precision Medicine for Chronic Heart Failure, Medical Innovation Research Division, Chinese PLA General Hospital Medical Big Data Research Center, Medical Innovation Research Division, Chinese PLA General HospitalAbstract Background Gut microbiota is significantly influenced by altitude. However, the dynamics of gut microbiota in relation to altitude remains undisclosed. Methods In this study, we investigated the microbiome profile of 610 healthy young men from three different places in China, grouped by altitude, duration of residence, and ethnicity. We conducted widely targeted metabolomic profiling and clinical testing to explore metabolic characteristics. Results Our findings revealed that as the Han individuals migrated from low altitude to high latitude, the gut microbiota gradually converged towards that of the Tibetan populations but reversed upon returning to lower altitude. Across different cohorts, we identified 51 species specifically enriched during acclimatization and 57 species enriched during deacclimatization to high altitude. Notably, Prevotella copri was found to be the most enriched taxon in both Tibetan and Han populations after ascending to high altitude. Furthermore, significant variations in host plasma metabolome and clinical indices at high altitude could be largely explained by changes in gut microbiota composition. Similar to Tibetans, 41 plasma metabolites, such as lactic acid, sphingosine-1-phosphate, taurine, and inositol, were significantly elevated in Han populations after ascending to high altitude. Germ-free animal experiments demonstrated that certain species, such as Escherichia coli and Klebsiella pneumoniae, which exhibited altitude-dependent variations in human populations, might play crucial roles in host purine metabolism. Conclusions This study provides insights into the dynamics of gut microbiota and host plasma metabolome with respect to altitude changes, indicating that their dynamics may have implications for host health at high altitude and contribute to host adaptation. Video Abstracthttps://doi.org/10.1186/s40168-024-01781-5Gut microbiotaAltitudeHypoxiaMetabolomePurine metabolism
spellingShingle Yang Han
Xiaoshuang Liu
Qian Jia
Jiayu Xu
Jinlong Shi
Xiang Li
Guotong Xie
Xiaojing Zhao
Kunlun He
Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
Microbiome
Gut microbiota
Altitude
Hypoxia
Metabolome
Purine metabolism
title Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
title_full Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
title_fullStr Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
title_full_unstemmed Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
title_short Longitudinal multi-omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
title_sort longitudinal multi omics analysis uncovers the altered landscape of gut microbiota and plasma metabolome in response to high altitude
topic Gut microbiota
Altitude
Hypoxia
Metabolome
Purine metabolism
url https://doi.org/10.1186/s40168-024-01781-5
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