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Sialidases and fucosidases of Akkermansia muciniphila are crucial for growth on mucin and nutrient sharing with mucus-associated gut bacteria

Author

Listed:
  • Bashar Shuoker

    (Technical University of Denmark
    Lund University)

  • Michael J. Pichler

    (Technical University of Denmark)

  • Chunsheng Jin

    (University of Gothenburg)

  • Hiroka Sakanaka

    (Technical University of Denmark)

  • Haiyang Wu

    (Quadram Institute Bioscience)

  • Ana Martínez Gascueña

    (Quadram Institute Bioscience)

  • Jining Liu

    (University of Gothenburg)

  • Tine Sofie Nielsen

    (Technical University of Denmark)

  • Jan Holgersson

    (University of Gothenburg)

  • Eva Nordberg Karlsson

    (Lund University)

  • Nathalie Juge

    (Quadram Institute Bioscience)

  • Sebastian Meier

    (Technical University of Denmark)

  • Jens Preben Morth

    (Technical University of Denmark)

  • Niclas G. Karlsson

    (University of Gothenburg)

  • Maher Abou Hachem

    (Technical University of Denmark)

Abstract

The mucolytic human gut microbiota specialist Akkermansia muciniphila is proposed to boost mucin-secretion by the host, thereby being a key player in mucus turnover. Mucin glycan utilization requires the removal of protective caps, notably fucose and sialic acid, but the enzymatic details of this process remain largely unknown. Here, we describe the specificities of ten A. muciniphila glycoside hydrolases, which collectively remove all known sialyl and fucosyl mucin caps including those on double-sulfated epitopes. Structural analyses revealed an unprecedented fucosidase modular arrangement and explained the sialyl T-antigen specificity of a sialidase of a previously unknown family. Cell-attached sialidases and fucosidases displayed mucin-binding and their inhibition abolished growth of A. muciniphila on mucin. Remarkably, neither the sialic acid nor fucose contributed to A. muciniphila growth, but instead promoted butyrate production by co-cultured Clostridia. This study brings unprecedented mechanistic insight into the initiation of mucin O-glycan degradation by A. muciniphila and nutrient sharing between mucus-associated bacteria.

Suggested Citation

  • Bashar Shuoker & Michael J. Pichler & Chunsheng Jin & Hiroka Sakanaka & Haiyang Wu & Ana Martínez Gascueña & Jining Liu & Tine Sofie Nielsen & Jan Holgersson & Eva Nordberg Karlsson & Nathalie Juge & , 2023. "Sialidases and fucosidases of Akkermansia muciniphila are crucial for growth on mucin and nutrient sharing with mucus-associated gut bacteria," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37533-6
    DOI: 10.1038/s41467-023-37533-6
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    1. Janneke Elzinga & Yoshiki Narimatsu & Noortje Haan & Henrik Clausen & Willem M. Vos & Hanne L. P. Tytgat, 2024. "Binding of Akkermansia muciniphila to mucin is O-glycan specific," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

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