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Glycan complexity dictates microbial resource allocation in the large intestine

Author

Listed:
  • Artur Rogowski

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Jonathon A. Briggs

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Jennifer C. Mortimer

    (University of Cambridge)

  • Theodora Tryfona

    (University of Cambridge)

  • Nicolas Terrapon

    (Architecture et Fonction des Macromolécules Biologiques (AFMB))

  • Elisabeth C. Lowe

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Arnaud Baslé

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Carl Morland

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Alison M. Day

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Hongjun Zheng

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Theresa E. Rogers

    (University of Michigan Medical School)

  • Paul Thompson

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Alastair R. Hawkins

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • Madhav P. Yadav

    (Eastern Regional Research Center)

  • Bernard Henrissat

    (Architecture et Fonction des Macromolécules Biologiques (AFMB)
    King Abdulaziz University)

  • Eric C. Martens

    (University of Michigan Medical School)

  • Paul Dupree

    (University of Cambridge)

  • Harry J. Gilbert

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

  • David N. Bolam

    (Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University)

Abstract

The structure of the human gut microbiota is controlled primarily through the degradation of complex dietary carbohydrates, but the extent to which carbohydrate breakdown products are shared between members of the microbiota is unclear. We show here, using xylan as a model, that sharing the breakdown products of complex carbohydrates by key members of the microbiota, such as Bacteroides ovatus, is dependent on the complexity of the target glycan. Characterization of the extensive xylan degrading apparatus expressed by B. ovatus reveals that the breakdown of the polysaccharide by the human gut microbiota is significantly more complex than previous models suggested, which were based on the deconstruction of xylans containing limited monosaccharide side chains. Our report presents a highly complex and dynamic xylan degrading apparatus that is fine-tuned to recognize the different forms of the polysaccharide presented to the human gut microbiota.

Suggested Citation

  • Artur Rogowski & Jonathon A. Briggs & Jennifer C. Mortimer & Theodora Tryfona & Nicolas Terrapon & Elisabeth C. Lowe & Arnaud Baslé & Carl Morland & Alison M. Day & Hongjun Zheng & Theresa E. Rogers &, 2015. "Glycan complexity dictates microbial resource allocation in the large intestine," Nature Communications, Nature, vol. 6(1), pages 1-16, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms8481
    DOI: 10.1038/ncomms8481
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    Citations

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    Cited by:

    1. Jennifer L. Modesto & Victoria H. Pearce & Guy E. Townsend, 2023. "Harnessing gut microbes for glycan detection and quantification," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Zihan Wang & Akshit Goyal & Veronika Dubinkina & Ashish B. George & Tong Wang & Yulia Fridman & Sergei Maslov, 2021. "Complementary resource preferences spontaneously emerge in diauxic microbial communities," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Ramón Verduzco-Oliva & Janet Alejandra Gutierrez-Uribe, 2020. "Beyond Enzyme Production: Solid State Fermentation (SSF) as an Alternative Approach to Produce Antioxidant Polysaccharides," Sustainability, MDPI, vol. 12(2), pages 1-14, January.
    4. Curtis Cottam & Rhys T. White & Lauren C. Beck & Christopher J. Stewart & Scott A. Beatson & Elisabeth C. Lowe & Rhys Grinter & James P. R. Connolly, 2024. "Metabolism of l-arabinose converges with virulence regulation to promote enteric pathogen fitness," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Itxaso Anso & Andreas Naegeli & Javier O. Cifuente & Ane Orrantia & Erica Andersson & Olatz Zenarruzabeitia & Alicia Moraleda-Montoya & Mikel García-Alija & Francisco Corzana & Rafael A. Orbe & Franci, 2023. "Turning universal O into rare Bombay type blood," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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