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Complex pectin metabolism by gut bacteria reveals novel catalytic functions

Author

Listed:
  • Didier Ndeh

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Artur Rogowski

    (Institute for Cell and Molecular Biosciences, Newcastle University
    †Present addresses: Megazyme, Bray, Co. Wicklow, A98 YV29, Ireland (A.R.); Institute for Wine Biotechnology, Department of Viticulture and Oenology, Stellenbosch University, Matieland 7602, South Africa (F.B.).)

  • Alan Cartmell

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Ana S. Luis

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Arnaud Baslé

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Joseph Gray

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Immacolata Venditto

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Jonathon Briggs

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Xiaoyang Zhang

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Aurore Labourel

    (Institute for Cell and Molecular Biosciences, Newcastle University)

  • Nicolas Terrapon

    (Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University)

  • Fanny Buffetto

    (INRA, UR1268 Biopolymères Interactions Assemblages
    †Present addresses: Megazyme, Bray, Co. Wicklow, A98 YV29, Ireland (A.R.); Institute for Wine Biotechnology, Department of Viticulture and Oenology, Stellenbosch University, Matieland 7602, South Africa (F.B.).)

  • Sergey Nepogodiev

    (John Innes Centre Norwich Research Park)

  • Yao Xiao

    (University of Michigan Medical School)

  • Robert A. Field

    (John Innes Centre Norwich Research Park)

  • Yanping Zhu

    (Complex Carbohydrate Research Center, The University of Georgia)

  • Malcolm A. O’Neill

    (Complex Carbohydrate Research Center, The University of Georgia)

  • Breeanna R. Urbanowicz

    (Complex Carbohydrate Research Center, The University of Georgia)

  • William S. York

    (Complex Carbohydrate Research Center, The University of Georgia)

  • Gideon J. Davies

    (University of York)

  • D. Wade Abbott

    (Lethbridge Research Centre)

  • Marie-Christine Ralet

    (INRA, UR1268 Biopolymères Interactions Assemblages)

  • Eric C. Martens

    (University of Michigan Medical School)

  • Bernard Henrissat

    (Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University
    INRA, USC 1408 AFMB
    King Abdulaziz University)

  • Harry J. Gilbert

    (Institute for Cell and Molecular Biosciences, Newcastle University)

Abstract

The metabolism of carbohydrate polymers drives microbial diversity in the human gut microbiota. It is unclear, however, whether bacterial consortia or single organisms are required to depolymerize highly complex glycans. Here we show that the gut bacterium Bacteroides thetaiotaomicron uses the most structurally complex glycan known: the plant pectic polysaccharide rhamnogalacturonan-II, cleaving all but 1 of its 21 distinct glycosidic linkages. The deconstruction of rhamnogalacturonan-II side chains and backbone are coordinated to overcome steric constraints, and the degradation involves previously undiscovered enzyme families and catalytic activities. The degradation system informs revision of the current structural model of rhamnogalacturonan-II and highlights how individual gut bacteria orchestrate manifold enzymes to metabolize the most challenging glycan in the human diet.

Suggested Citation

  • Didier Ndeh & Artur Rogowski & Alan Cartmell & Ana S. Luis & Arnaud Baslé & Joseph Gray & Immacolata Venditto & Jonathon Briggs & Xiaoyang Zhang & Aurore Labourel & Nicolas Terrapon & Fanny Buffetto &, 2017. "Complex pectin metabolism by gut bacteria reveals novel catalytic functions," Nature, Nature, vol. 544(7648), pages 65-70, April.
    • Handle: RePEc:nat:nature:v:544:y:2017:i:7648:d:10.1038_nature21725
    DOI: 10.1038/nature21725
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    Cited by:

    1. Yonggan Sun & Qixing Nie & Shanshan Zhang & Huijun He & Sheng Zuo & Chunhua Chen & Jingrui Yang & Haihong Chen & Jielun Hu & Song Li & Jiaobo Cheng & Baojie Zhang & Zhitian Zheng & Shijie Pan & Ping H, 2023. "Parabacteroides distasonis ameliorates insulin resistance via activation of intestinal GPR109a," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Erika C. Freeman & Erik J. S. Emilson & Thorsten Dittmar & Lucas P. P. Braga & Caroline E. Emilson & Tobias Goldhammer & Christine Martineau & Gabriel Singer & Andrew J. Tanentzap, 2024. "Universal microbial reworking of dissolved organic matter along environmental gradients," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Alei Geng & Nana Li & Anaiza Zayas-Garriga & Rongrong Xie & Daochen Zhu & Jianzhong Sun, 2024. "Direct Conversion of Minimally Pretreated Corncob by Enzyme-Intensified Microbial Consortia," Agriculture, MDPI, vol. 14(9), pages 1-13, September.
    4. Hao-Tian Wang & Zi-Long Wang & Kuan Chen & Ming-Ju Yao & Meng Zhang & Rong-Shen Wang & Jia-He Zhang & Hans Ågren & Fu-Dong Li & Junhao Li & Xue Qiao & Min Ye, 2023. "Insights into the missing apiosylation step in flavonoid apiosides biosynthesis of Leguminosae plants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Stefan Dyksma & Michael Pester, 2023. "Oxygen respiration and polysaccharide degradation by a sulfate-reducing acidobacterium," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Diego E. Sastre & Nazneen Sultana & Marcos V. A. S. Navarro & Maros Huliciak & Jonathan Du & Javier O. Cifuente & Maria Flowers & Xu Liu & Pete Lollar & Beatriz Trastoy & Marcelo E. Guerin & Eric J. S, 2024. "Human gut microbes express functionally distinct endoglycosidases to metabolize the same N-glycan substrate," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. María Ángeles Rivas & Rocío Casquete & Alberto Martín & María de Guía Córdoba & Emilio Aranda & María José Benito, 2021. "Strategies to Increase the Biological and Biotechnological Value of Polysaccharides from Agricultural Waste for Application in Healthy Nutrition," IJERPH, MDPI, vol. 18(11), pages 1-19, June.

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