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Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Author

Listed:
  • Fiona Cuskin

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
    Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA)

  • Elisabeth C. Lowe

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK)

  • Max J. Temple

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK)

  • Yanping Zhu

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
    Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA)

  • Elizabeth A. Cameron

    (University of Michigan Medical School)

  • Nicholas A. Pudlo

    (University of Michigan Medical School)

  • Nathan T. Porter

    (University of Michigan Medical School)

  • Karthik Urs

    (University of Michigan Medical School)

  • Andrew J. Thompson

    (University of York, York YO10 5DD, UK)

  • Alan Cartmell

    (School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne)

  • Artur Rogowski

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK)

  • Brian S. Hamilton

    (Interdisciplinary Biochemistry Graduate Program, Indiana University, 800 E. Kirkwood Avenue, Bloomington, Indiana 47405, USA)

  • Rui Chen

    (Indiana University, 800 E. Kirkwood Avenue, Bloomington, Indiana 47405, USA)

  • Thomas J. Tolbert

    (University of Kansas School of Pharmacy, 2095 Constant Avenue, Lawrence, Kansas 66047, USA)

  • Kathleen Piens

    (Oxyrane, 9052 Ghent, Belgium)

  • Debby Bracke

    (Oxyrane, 9052 Ghent, Belgium)

  • Wouter Vervecken

    (Oxyrane, 9052 Ghent, Belgium)

  • Zalihe Hakki

    (School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne)

  • Gaetano Speciale

    (School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne)

  • Jose L. Munōz-Munōz

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK)

  • Andrew Day

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK)

  • Maria J. Peña

    (Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA)

  • Richard McLean

    (Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, Alberta T1J 4B1, Canada)

  • Michael D. Suits

    (Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia V8P 5C2, Canada)

  • Alisdair B. Boraston

    (Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia V8P 5C2, Canada)

  • Todd Atherly

    (USDA, Agricultural Research Service, National Laboratory for Agriculture and the Environment, Ames, Iowa 50011, USA)

  • Cherie J. Ziemer

    (USDA, Agricultural Research Service, National Laboratory for Agriculture and the Environment, Ames, Iowa 50011, USA)

  • Spencer J. Williams

    (School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne)

  • Gideon J. Davies

    (University of York, York YO10 5DD, UK)

  • D. Wade Abbott

    (Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA
    Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, Alberta T1J 4B1, Canada)

  • Eric C. Martens

    (University of Michigan Medical School)

  • Harry J. Gilbert

    (Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
    Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA)

Abstract

Yeasts, which have been a component of the human diet for at least 7,000 years, possess an elaborate cell wall α-mannan. The influence of yeast mannan on the ecology of the human microbiota is unknown. Here we show that yeast α-mannan is a viable food source for the Gram-negative bacterium Bacteroides thetaiotaomicron, a dominant member of the microbiota. Detailed biochemical analysis and targeted gene disruption studies support a model whereby limited cleavage of α-mannan on the surface generates large oligosaccharides that are subsequently depolymerized to mannose by the action of periplasmic enzymes. Co-culturing studies showed that metabolism of yeast mannan by B. thetaiotaomicron presents a ‘selfish’ model for the catabolism of this difficult to breakdown polysaccharide. Genomic comparison with B. thetaiotaomicron in conjunction with cell culture studies show that a cohort of highly successful members of the microbiota has evolved to consume sterically-restricted yeast glycans, an adaptation that may reflect the incorporation of eukaryotic microorganisms into the human diet.

Suggested Citation

  • Fiona Cuskin & Elisabeth C. Lowe & Max J. Temple & Yanping Zhu & Elizabeth A. Cameron & Nicholas A. Pudlo & Nathan T. Porter & Karthik Urs & Andrew J. Thompson & Alan Cartmell & Artur Rogowski & Brian, 2015. "Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism," Nature, Nature, vol. 517(7533), pages 165-169, January.
    • Handle: RePEc:nat:nature:v:517:y:2015:i:7533:d:10.1038_nature13995
    DOI: 10.1038/nature13995
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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. Omar Al-Jourani & Samuel T. Benedict & Jennifer Ross & Abigail J. Layton & Phillip Peet & Victoria M. Marando & Nicholas P. Bailey & Tiaan Heunis & Joseph Manion & Francesca Mensitieri & Aaron Frankli, 2023. "Identification of d-arabinan-degrading enzymes in mycobacteria," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Aaron Franklin & Vivian C. Salgueiro & Abigail J. Layton & Rudi Sullivan & Todd Mize & Lucía Vázquez-Iniesta & Samuel T. Benedict & Sudagar S. Gurcha & Itxaso Anso & Gurdyal S. Besra & Manuel Banzhaf , 2024. "The mycobacterial glycoside hydrolase LamH enables capsular arabinomannan release and stimulates growth," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Alicia E. Graham & Rodrigo Ledesma-Amaro, 2023. "The microbial food revolution," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    5. Lharbi Dridi & Fernando Altamura & Emmanuel Gonzalez & Olivia Lui & Ryszard Kubinski & Reilly Pidgeon & Adrian Montagut & Jasmine Chong & Jianguo Xia & Corinne F. Maurice & Bastien Castagner, 2023. "Identifying glycan consumers in human gut microbiota samples using metabolic labeling coupled with fluorescence-activated cell sorting," Nature Communications, Nature, vol. 14(1), pages 1-13, 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.

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