Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study
Background The importance of gut microbes in mediating the benefits of lifestyle intervention is increasingly recognized. However, compared to the bacterial microbiome, the role of intestinal fungi in exercise remains elusive. With our established randomized controlled trial of exercise intervention...
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Taylor & Francis Group
2024-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2024.2416928 |
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| author | Yao Wang Jiarui Chen Yueqiong Ni Yan Liu Xiang Gao Michael Andrew Tse Gianni Panagiotou Aimin Xu |
| author_facet | Yao Wang Jiarui Chen Yueqiong Ni Yan Liu Xiang Gao Michael Andrew Tse Gianni Panagiotou Aimin Xu |
| author_sort | Yao Wang |
| collection | DOAJ |
| description | Background The importance of gut microbes in mediating the benefits of lifestyle intervention is increasingly recognized. However, compared to the bacterial microbiome, the role of intestinal fungi in exercise remains elusive. With our established randomized controlled trial of exercise intervention in Chinese males with prediabetes (n = 39, ClinicalTrials.gov:NCT03240978), we investigated the dynamics of human gut mycobiome and further interrogated their associations with exercise-elicited outcomes using multi-omics approaches.Methods Clinical variations and biological samples were collected before and after training. Fecal fungal composition was analyzed using the internal transcribed spacer 2 (ITS2) sequencing and integrated with paired shotgun metagenomics, untargeted metabolomics, and Olink proteomics.Results Twelve weeks of exercise training profoundly promoted fungal ecological diversity and intrakingdom connection. We further identified exercise-responsive genera with potential metabolic benefits, including Verticillium, Sarocladium, and Ceratocystis. Using multi-omics approaches, we elucidated comprehensive associations between changes in gut mycobiome and exercise-shaped metabolic phenotypes, bacterial microbiome, and circulating metabolomics and proteomics profiles. Furthermore, a machine-learning algorithm built using baseline microbial signatures and clinical characteristics predicted exercise responsiveness in improvements of insulin sensitivity, with an area under the receiver operating characteristic (AUROC) of 0.91 (95% CI: 0.85–0.97) in the discovery cohort and of 0.79 (95% CI: 0.74–0.86) in the independent validation cohort (n = 30).Conclusions Our findings suggest that intense exercise training significantly remodels the human fungal microbiome composition. Changes in gut fungal composition are associated with the metabolic benefits of exercise, indicating gut mycobiome is a possible molecular transducer of exercise. Moreover, baseline gut fungal signatures predict exercise responsiveness for diabetes prevention, highlighting that targeting the gut mycobiome emerges as a prospective strategy in tailoring personalized training for diabetes prevention. |
| format | Article |
| id | doaj-art-1087ce547a31400ea5ba09a61cf39aab |
| institution | OA Journals |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-1087ce547a31400ea5ba09a61cf39aab2025-08-20T02:29:59ZengTaylor & Francis GroupGut Microbes1949-09761949-09842024-12-0116110.1080/19490976.2024.2416928Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics studyYao Wang0Jiarui Chen1Yueqiong Ni2Yan Liu3Xiang Gao4Michael Andrew Tse5Gianni Panagiotou6Aimin Xu7State Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaState Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaDepartment of Microbiome Dynamics, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knoll Institute, Jena, GermanyState Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaState Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaState Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaState Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaState Key Laboratory of Pharmaceutical Biotechnology, The University of Hong Kong, Hong Kong, ChinaBackground The importance of gut microbes in mediating the benefits of lifestyle intervention is increasingly recognized. However, compared to the bacterial microbiome, the role of intestinal fungi in exercise remains elusive. With our established randomized controlled trial of exercise intervention in Chinese males with prediabetes (n = 39, ClinicalTrials.gov:NCT03240978), we investigated the dynamics of human gut mycobiome and further interrogated their associations with exercise-elicited outcomes using multi-omics approaches.Methods Clinical variations and biological samples were collected before and after training. Fecal fungal composition was analyzed using the internal transcribed spacer 2 (ITS2) sequencing and integrated with paired shotgun metagenomics, untargeted metabolomics, and Olink proteomics.Results Twelve weeks of exercise training profoundly promoted fungal ecological diversity and intrakingdom connection. We further identified exercise-responsive genera with potential metabolic benefits, including Verticillium, Sarocladium, and Ceratocystis. Using multi-omics approaches, we elucidated comprehensive associations between changes in gut mycobiome and exercise-shaped metabolic phenotypes, bacterial microbiome, and circulating metabolomics and proteomics profiles. Furthermore, a machine-learning algorithm built using baseline microbial signatures and clinical characteristics predicted exercise responsiveness in improvements of insulin sensitivity, with an area under the receiver operating characteristic (AUROC) of 0.91 (95% CI: 0.85–0.97) in the discovery cohort and of 0.79 (95% CI: 0.74–0.86) in the independent validation cohort (n = 30).Conclusions Our findings suggest that intense exercise training significantly remodels the human fungal microbiome composition. Changes in gut fungal composition are associated with the metabolic benefits of exercise, indicating gut mycobiome is a possible molecular transducer of exercise. Moreover, baseline gut fungal signatures predict exercise responsiveness for diabetes prevention, highlighting that targeting the gut mycobiome emerges as a prospective strategy in tailoring personalized training for diabetes prevention.https://www.tandfonline.com/doi/10.1080/19490976.2024.2416928Gut mycobiomefungal microbiomeexercise trainingdiabetes preventionmulti-omicsrandomized controlled trial |
| spellingShingle | Yao Wang Jiarui Chen Yueqiong Ni Yan Liu Xiang Gao Michael Andrew Tse Gianni Panagiotou Aimin Xu Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study Gut Microbes Gut mycobiome fungal microbiome exercise training diabetes prevention multi-omics randomized controlled trial |
| title | Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study |
| title_full | Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study |
| title_fullStr | Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study |
| title_full_unstemmed | Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study |
| title_short | Exercise-changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention: an integrative multi-omics study |
| title_sort | exercise changed gut mycobiome as a potential contributor to metabolic benefits in diabetes prevention an integrative multi omics study |
| topic | Gut mycobiome fungal microbiome exercise training diabetes prevention multi-omics randomized controlled trial |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2024.2416928 |
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