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A single sulfatase is required to access colonic mucin by a gut bacterium

Author

Listed:
  • Ana S. Luis

    (University of Michigan
    University of Gothenburg)

  • Chunsheng Jin

    (University of Gothenburg)

  • Gabriel Vasconcelos Pereira

    (University of Michigan)

  • Robert W. P. Glowacki

    (University of Michigan)

  • Sadie R. Gugel

    (University of Michigan)

  • Shaleni Singh

    (University of Michigan)

  • Dominic P. Byrne

    (University of Liverpool)

  • Nicholas A. Pudlo

    (University of Michigan)

  • James A. London

    (University of Liverpool)

  • Arnaud Baslé

    (Newcastle University)

  • Mark Reihill

    (University College Dublin, Belfield)

  • Stefan Oscarson

    (University College Dublin, Belfield)

  • Patrick A. Eyers

    (University of Liverpool)

  • Mirjam Czjzek

    (Sorbonne Université, Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models)

  • Gurvan Michel

    (Sorbonne Université, Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models)

  • Tristan Barbeyron

    (Sorbonne Université, Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models)

  • Edwin A. Yates

    (University of Liverpool)

  • Gunnar C. Hansson

    (University of Gothenburg)

  • Niclas G. Karlsson

    (University of Gothenburg)

  • Alan Cartmell

    (University of Liverpool)

  • Eric C. Martens

    (University of Michigan)

Abstract

Humans have co-evolved with a dense community of microbial symbionts that inhabit the lower intestine. In the colon, secreted mucus creates a barrier that separates these microorganisms from the intestinal epithelium1. Some gut bacteria are able to utilize mucin glycoproteins, the main mucus component, as a nutrient source. However, it remains unclear which bacterial enzymes initiate degradation of the complex O-glycans found in mucins. In the distal colon, these glycans are heavily sulfated, but specific sulfatases that are active on colonic mucins have not been identified. Here we show that sulfatases are essential to the utilization of distal colonic mucin O-glycans by the human gut symbiont Bacteroides thetaiotaomicron. We characterized the activity of 12 different sulfatases produced by this species, showing that they are collectively active on all known sulfate linkages in O-glycans. Crystal structures of three enzymes provide mechanistic insight into the molecular basis of substrate specificity. Unexpectedly, we found that a single sulfatase is essential for utilization of sulfated O-glycans in vitro and also has a major role in vivo. Our results provide insight into the mechanisms of mucin degradation by a prominent group of gut bacteria, an important process for both normal microbial gut colonization2 and diseases such as inflammatory bowel disease3.

Suggested Citation

  • Ana S. Luis & Chunsheng Jin & Gabriel Vasconcelos Pereira & Robert W. P. Glowacki & Sadie R. Gugel & Shaleni Singh & Dominic P. Byrne & Nicholas A. Pudlo & James A. London & Arnaud Baslé & Mark Reihil, 2021. "A single sulfatase is required to access colonic mucin by a gut bacterium," Nature, Nature, vol. 598(7880), pages 332-337, October.
  • Handle: RePEc:nat:nature:v:598:y:2021:i:7880:d:10.1038_s41586-021-03967-5
    DOI: 10.1038/s41586-021-03967-5
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    Citations

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    Cited by:

    1. Daniel P. G. H. Wong & Benjamin H. Good, 2024. "Quantifying the adaptive landscape of commensal gut bacteria using high-resolution lineage tracking," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Sandra M. Holmberg & Rachel H. Feeney & Vishnu Prasoodanan P.K. & Fabiola Puértolas-Balint & Dhirendra K. Singh & Supapit Wongkuna & Lotte Zandbergen & Hans Hauner & Beate Brandl & Anni I. Nieminen & , 2024. "The gut commensal Blautia maintains colonic mucus function under low-fiber consumption through secretion of short-chain fatty acids," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. 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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