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Binding of Akkermansia muciniphila to mucin is O-glycan specific

Author

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  • Janneke Elzinga

    (Wageningen University & Research
    Faculty of Health Sciences, University of Copenhagen)

  • Yoshiki Narimatsu

    (Faculty of Health Sciences, University of Copenhagen
    GlycoDisplay ApS)

  • Noortje Haan

    (Faculty of Health Sciences, University of Copenhagen
    Leiden University Medical Center)

  • Henrik Clausen

    (Faculty of Health Sciences, University of Copenhagen)

  • Willem M. Vos

    (Wageningen University & Research
    Faculty of Medicine, University of Helsinki)

  • Hanne L. P. Tytgat

    (Wageningen University & Research
    Nestlé Research)

Abstract

The intestinal anaerobic bacterium Akkermansia muciniphila is specialized in the degradation of mucins, which are heavily O-glycosylated proteins that constitute the major components of the mucus lining the intestine. Despite that adhesion to mucins is considered critical for the persistence of A. muciniphila in the human intestinal tract, our knowledge of how this intestinal symbiont recognizes and binds to mucins is still limited. Here, we first show that the mucin-binding properties of A. muciniphila are independent of environmental oxygen concentrations and not abolished by pasteurization. We then dissected the mucin-binding properties of pasteurized A. muciniphila by use of a recently developed cell-based mucin array that enables display of the tandem repeats of human mucins with distinct O-glycan patterns and structures. We found that A. muciniphila recognizes the unsialylated LacNAc (Galβ1-4GlcNAcβ1-R) disaccharide selectively on core2 and core3 O-glycans. This disaccharide epitope is abundantly found on human colonic mucins capped by sialic acids, and we demonstrated that endogenous A. muciniphila neuraminidase activity can uncover the epitope and promote binding. In summary, our study provides insights into the mucin-binding properties important for colonization of a key mucin-foraging bacterium.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48770-8
    DOI: 10.1038/s41467-024-48770-8
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    1. Louise E. Tailford & C. David Owen & John Walshaw & Emmanuelle H. Crost & Jemma Hardy-Goddard & Gwenaelle Le Gall & Willem M. de Vos & Garry L. Taylor & Nathalie Juge, 2015. "Discovery of intramolecular trans-sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
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    5. Rebecca Nason & Christian Büll & Andriana Konstantinidi & Lingbo Sun & Zilu Ye & Adnan Halim & Wenjuan Du & Daniel M. Sørensen & Fabien Durbesson & Sanae Furukawa & Ulla Mandel & Hiren J. Joshi & Leo , 2021. "Display of the human mucinome with defined O-glycans by gene engineered cells," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    6. 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.
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