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The gut microbiota drives aging-related erythropoiesis impairment via phenylacetic acid–induced histone phenylacetylation

  • Yifei Xie
  • , Xiangrui Qiao
  • , Hao Wu
  • , Yiming Hua
  • , Bolin Li
  • , Ning Ding
  • , Jinglong Pang
  • , Mingmin Zhang
  • , Wen Xi
  • , Kai Deng
  • , Yu Xu
  • , Peining Liu
  • , Xue Shi
  • , Lele Cheng
  • , Xiaozhen Zhuo
  • , Ting Li
  • , Zuyi Yuan
  • , Yue Wu
  • Department of Cardiovascular Medicine
  • The First Affiliated Hospital of Xi’an Jiaotong University
  • Key Laboratory of Molecular Cardiology
  • Key Laboratory of Environment and Genes Related to Diseases
  • Key Lab of the Ministry of Education for Process Control and Efficiency Egineering
  • Department of Cardiology
  • Southwest Jiaotong University
  • Department of Clinical Laboratory
  • Department of Medical Imaging

Research output: Contribution to journal › Article › peer-review

Abstract

Anemia, the most prevalent hematologic disorder in older adults, imposes a significant burden of cardiovascular events, cognitive decline, and mortality. However, the mechanisms underlying aging-related anemia, especially epigenetic dysregulation in hematopoietic stem and progenitor cells (HSPCs), remain incompletely understood. Although the gut microbiota is critical for hematopoiesis, its specific contribution to aging-related erythropoiesis impairment remains unclear. Here, we reveal that aging markedly activates phenylalanine metabolism and elevates plasma phenylacetic acid (PAA) levels in both humans and mice. We identify Odoribacter splanchnicus (O splanchnicus) as a key gut symbiont whose abundance is significantly increased in aged mice and which directly drives PAA production from phenylalanine via the 2-oxoacid:ferredoxin oxidoreductase superfamily encoded by porA, nifJ, and iorA/iorB. Rifaximin treatment selectively reduces O splanchnicus and plasma PAA, thereby alleviating aging-related anemia. Mechanistically, PAA promotes a novel posttranslational modification termed histone lysine phenylacetylation (Kpa) through the acetyltransferase histone acetyltransferase binding to origin recognition complex 1 (HBO1). Elevated histone Kpa increases chromatin accessibility at the GATA2 promoter, disrupts the GATA switch, and blocks erythroid differentiation of HSPCs. In vivo, supplementation with sodium phenylacetate exacerbates anemia in microbiota-depleted mice, whereas the HBO1 inhibitor WM-3835 restores erythropoiesis by reversing histone Kpa and normalizing the GATA switch. Furthermore, dietary phenylalanine restriction lowers circulating PAA and effectively ameliorates aging-related anemia in both naturally aged mice and O splanchnicus–colonized mice. These findings provide, to our knowledge, the first evidence that gut microbiota–derived PAA plays a critical role in the development of aging-related erythropoiesis impairment and offer multiple translatable strategies for treating this condition.

Original languageEnglish
JournalBlood
DOIs
StateAccepted/In press - 2026
Externally publishedYes

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