Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway

Radiation-associated hematopoietic recovery (RAHR) is critical for mitigating lethal complications of acute radiation syndrome (ARS), yet therapeutic strategies remain limited. Through integrated multi-omics analysis of a total body irradiation (TBI) mouse model, we identify Bacteroides acidifaciens...

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Main Authors: Yang Jiao, Jiawei Ren, Shichang Xie, Nan Yuan, Jiaqi Shen, Huafang Yin, Jian Wang, Hongjuan Guo, Jianping Cao, Xin Wang, Depei Wu, Zhemin Zhou, Xiaofei Qi
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2025.2488105
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author Yang Jiao
Jiawei Ren
Shichang Xie
Nan Yuan
Jiaqi Shen
Huafang Yin
Jian Wang
Hongjuan Guo
Jianping Cao
Xin Wang
Depei Wu
Zhemin Zhou
Xiaofei Qi
author_facet Yang Jiao
Jiawei Ren
Shichang Xie
Nan Yuan
Jiaqi Shen
Huafang Yin
Jian Wang
Hongjuan Guo
Jianping Cao
Xin Wang
Depei Wu
Zhemin Zhou
Xiaofei Qi
author_sort Yang Jiao
collection DOAJ
description Radiation-associated hematopoietic recovery (RAHR) is critical for mitigating lethal complications of acute radiation syndrome (ARS), yet therapeutic strategies remain limited. Through integrated multi-omics analysis of a total body irradiation (TBI) mouse model, we identify Bacteroides acidifaciens-dominated gut microbiota as key mediators of RAHR impairment. 16S ribosomal rRNA sequencing revealed TBI-induced dysbiosis characterized by Bacteroidaceae enrichment, while functional metagenomics identified raffinose metabolism as the most significantly perturbed pathway. Notably, raffinose supplementation (10% w/v) recapitulated radiation-induced microbiota shifts and delayed bone marrow recovery. Fecal microbiota transplantation (FMT) revealed a causative role for raffinose-metabolizing microbiota, particularly Bacteroides acidifaciens, in delaying RAHR progression. Mechanistically, B. acidifaciens-mediated bile acid deconjugation activated FXR, subsequently suppressing NF-κB-dependent hematopoietic recovery. Therapeutic FXR inhibition via ursodeoxycholic acid (UDCA) had been shown to be a viable method for rescuing RAHR. Our results delineated a microbiome-bile acid-FXR axis as a master regulator of post-irradiation hematopoiesis. Targeting B. acidifaciens or its metabolic derivatives could represent a translatable strategy to mitigate radiation-induced hematopoietic injury.
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spelling doaj-art-af3e8a73dbee48f9a2da594898ee94082025-08-20T02:08:12ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2025.2488105Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathwayYang Jiao0Jiawei Ren1Shichang Xie2Nan Yuan3Jiaqi Shen4Huafang Yin5Jian Wang6Hongjuan Guo7Jianping Cao8Xin Wang9Depei Wu10Zhemin Zhou11Xiaofei Qi12State Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaKey Laboratory of Alkene-Carbon Fibers-Based Technology & Application for Detection of Major Infectious Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Cancer Institute, Suzhou Medical College, Soochow University, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaThe Affiliated Jiangyin People’s Hospital of Nantong University, Jiangyin, ChinaThe Affiliated Jiangyin People’s Hospital of Nantong University, Jiangyin, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products & Institute of Food Sciences, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory of Radiation Medicine and Protection, School of Radiation Medicine and Protection, Soochow University, Suzhou, ChinaKey Laboratory of Alkene-Carbon Fibers-Based Technology & Application for Detection of Major Infectious Diseases, MOE Key Laboratory of Geriatric Diseases and Immunology, Cancer Institute, Suzhou Medical College, Soochow University, Suzhou, ChinaNational Clinical Research Center for Hematologic Diseases, Jiangsu Institute of Hematology, Collaborative Innovation Center of Hematology, Suzhou, ChinaRadiation-associated hematopoietic recovery (RAHR) is critical for mitigating lethal complications of acute radiation syndrome (ARS), yet therapeutic strategies remain limited. Through integrated multi-omics analysis of a total body irradiation (TBI) mouse model, we identify Bacteroides acidifaciens-dominated gut microbiota as key mediators of RAHR impairment. 16S ribosomal rRNA sequencing revealed TBI-induced dysbiosis characterized by Bacteroidaceae enrichment, while functional metagenomics identified raffinose metabolism as the most significantly perturbed pathway. Notably, raffinose supplementation (10% w/v) recapitulated radiation-induced microbiota shifts and delayed bone marrow recovery. Fecal microbiota transplantation (FMT) revealed a causative role for raffinose-metabolizing microbiota, particularly Bacteroides acidifaciens, in delaying RAHR progression. Mechanistically, B. acidifaciens-mediated bile acid deconjugation activated FXR, subsequently suppressing NF-κB-dependent hematopoietic recovery. Therapeutic FXR inhibition via ursodeoxycholic acid (UDCA) had been shown to be a viable method for rescuing RAHR. Our results delineated a microbiome-bile acid-FXR axis as a master regulator of post-irradiation hematopoiesis. Targeting B. acidifaciens or its metabolic derivatives could represent a translatable strategy to mitigate radiation-induced hematopoietic injury.https://www.tandfonline.com/doi/10.1080/19490976.2025.2488105Radiation-induced hematopoietic injurygut microbiomeBacteroides acidifaciensraffinose-metabolizing bacteriaIntestinal-Hematopoietic AxisUDCA
spellingShingle Yang Jiao
Jiawei Ren
Shichang Xie
Nan Yuan
Jiaqi Shen
Huafang Yin
Jian Wang
Hongjuan Guo
Jianping Cao
Xin Wang
Depei Wu
Zhemin Zhou
Xiaofei Qi
Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway
Gut Microbes
Radiation-induced hematopoietic injury
gut microbiome
Bacteroides acidifaciens
raffinose-metabolizing bacteria
Intestinal-Hematopoietic Axis
UDCA
title Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway
title_full Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway
title_fullStr Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway
title_full_unstemmed Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway
title_short Raffinose-metabolizing bacteria impair radiation-associated hematopoietic recovery via the bile acid/FXR/NF-κB signaling pathway
title_sort raffinose metabolizing bacteria impair radiation associated hematopoietic recovery via the bile acid fxr nf κb signaling pathway
topic Radiation-induced hematopoietic injury
gut microbiome
Bacteroides acidifaciens
raffinose-metabolizing bacteria
Intestinal-Hematopoietic Axis
UDCA
url https://www.tandfonline.com/doi/10.1080/19490976.2025.2488105
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