IDEAS home Printed from https://ideas.repec.org/a/nat/nature/v517y2015i7533d10.1038_nature13995.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/nature13995
    File Function: Abstract
    Download Restriction: Access to the full text of the articles in this series is restricted.
    File URL: https://libkey.io/10.1038/nature13995?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    As the access to this document is restricted, you may want to search for a different version of it.

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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. 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.
    5. 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.
    6. Alicia E. Graham & Rodrigo Ledesma-Amaro, 2023. "The microbial food revolution," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:nature:v:517:y:2015:i:7533:d:10.1038_nature13995. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    We have no bibliographic references for this item. You can help adding them by using this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.