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

Gut Microbes. 2025 Dec;17(1):2488105. doi: 10.1080/19490976.2025.2488105. Epub 2025 Apr 7.

Abstract

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.

Keywords: Bacteroides acidifaciens; FXR; Intestinal-Hematopoietic Axis; Radiation-induced hematopoietic injury; UDCA; gut microbiome; raffinose-metabolizing bacteria.

MeSH terms

  • Acute Radiation Syndrome* / metabolism
  • Acute Radiation Syndrome* / microbiology
  • Animals
  • Bacteria* / classification
  • Bacteria* / genetics
  • Bacteria* / isolation & purification
  • Bacteria* / metabolism
  • Bile Acids and Salts* / metabolism
  • Dysbiosis / microbiology
  • Fecal Microbiota Transplantation
  • Gastrointestinal Microbiome* / radiation effects
  • Hematopoiesis* / radiation effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-kappa B* / genetics
  • NF-kappa B* / metabolism
  • Raffinose* / metabolism
  • Receptors, Cytoplasmic and Nuclear* / genetics
  • Receptors, Cytoplasmic and Nuclear* / metabolism
  • Signal Transduction / radiation effects
  • Whole-Body Irradiation / adverse effects

Substances

  • Bile Acids and Salts
  • NF-kappa B
  • Raffinose
  • Receptors, Cytoplasmic and Nuclear