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<p>Dietary proanthocyanidins (PACs) are polyphenols that promote a healthy gut microbiome. PACs are notable for their rich catechol moieties with high affinity for iron, enabling them to interfere with pathogens’ iron uptake. PACs selectively increase the abundance of <i>Akkermansia muciniphila</i>, a symbiont known for supporting metabolic and immune health. We discovered that <i>A. muciniphila</i> Muc<sup>T</sup> utilizes distinct iron-acquisition systems to take up iron sequestered by PACs, supporting its metabolic activity. Integrative proteomics and transcriptomics revealed that <i>A. muciniphila</i> has an active catechol-type siderophore-mediated iron uptake (Fe<sup>3+</sup>) system, involving membrane ATP-binding cassette transporters and lipocalins. Simultaneously, the expression of ferrous iron (Fe<sup>2+</sup>) transporters, zinc uptake, and iron storage proteins was upregulated. Administering iron-laden PACs in an iron-depleted medium restored the <i>A. muciniphila</i> growth to levels comparable to those in iron-amended conditions. This was associated with an increased expression of the <i>A. muciniphila</i> siderophore operon and lipocalin genes, indicating that iron-laden PACs are recognized as xenosiderophores to cope with iron depletion. Hence, we identified novel signaling mechanisms for iron acquisition and siderophore uptake regulation in <i>A. muciniphila</i> Muc<sup>T</sup> upon exposure to PACs, enhancing our understanding of the role of dietary PACs in selectively promoting this gut symbiont and potentially outcompeting pathogenic bacteria.</p>

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Akkermansia muciniphila MucT harnesses dietary polyphenols as xenosiderophores for enhanced iron uptake

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年10月24日

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  • Maria-Carolina Rodríguez-Daza,
  • Sjef Boeren,
  • Hanne L. P. Tytgat,
  • Yves Desjardins,
  • Willem M. de Vos

摘要

Dietary proanthocyanidins (PACs) are polyphenols that promote a healthy gut microbiome. PACs are notable for their rich catechol moieties with high affinity for iron, enabling them to interfere with pathogens’ iron uptake. PACs selectively increase the abundance of Akkermansia muciniphila, a symbiont known for supporting metabolic and immune health. We discovered that A. muciniphila MucT utilizes distinct iron-acquisition systems to take up iron sequestered by PACs, supporting its metabolic activity. Integrative proteomics and transcriptomics revealed that A. muciniphila has an active catechol-type siderophore-mediated iron uptake (Fe3+) system, involving membrane ATP-binding cassette transporters and lipocalins. Simultaneously, the expression of ferrous iron (Fe2+) transporters, zinc uptake, and iron storage proteins was upregulated. Administering iron-laden PACs in an iron-depleted medium restored the A. muciniphila growth to levels comparable to those in iron-amended conditions. This was associated with an increased expression of the A. muciniphila siderophore operon and lipocalin genes, indicating that iron-laden PACs are recognized as xenosiderophores to cope with iron depletion. Hence, we identified novel signaling mechanisms for iron acquisition and siderophore uptake regulation in A. muciniphila MucT upon exposure to PACs, enhancing our understanding of the role of dietary PACs in selectively promoting this gut symbiont and potentially outcompeting pathogenic bacteria.