Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

  • Nature. 2015 Jan 8;517(7533):165-169. doi: 10.1038/nature13995.
Fiona Cuskin  #  1  2 ,  Elisabeth C Lowe  #  1 ,  Max J Temple  #  1 ,  Yanping Zhu  1  2 ,  Elizabeth Cameron  3 ,  Nicholas A Pudlo  3 ,  Nathan T Porter  3 ,  Karthik Urs  3 ,  Andrew J Thompson  4 ,  Alan Cartmell  5 ,  Artur Rogowski  1 ,  Brian S Hamilton  6 ,  Rui Chen  6 ,  Thomas J Tolbert  6 ,  Kathleen Piens  7 ,  Debby Bracke  7 ,  Wouter Vervecken  7 ,  Zalihe Hakki  5 ,  Gaetano Speciale  5 ,  Jose L Munōz-Munōz  1 ,  Andrew Day  1 ,  Maria J Peña  2 ,  Richard McLean  8 ,  Michael D Suits  9 ,  Alisdair B Boraston  9 ,  Todd Atherly  10 ,  Cherie J Ziemer  10 ,  Spencer J Williams  5 ,  Gideon J Davies  4 ,  D Wade Abbott  2  8 ,  Eric C Martens  3 ,  Harry J Gilbert  1  2
Affiliations
  • 1. Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
  • 2. Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, GA 30602, USA.
  • 3. Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI, USA.
  • 4. Department of Chemistry, University of York, York YO10 5DD, U.K.
  • 5. School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria 3010, Australia.
  • 6. Dept. of Pharmaceutical Chemistry, University of Kansas School of Pharmacy, 2095 Constant Ave, Lawrence, KS 66047, USA.
  • 7. Oxyrane, Ghent, Belgium.
  • 8. Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, AB, Canada.
  • 9. Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada.
  • 10. USDA, Agricultural Research Service, National Laboratory for Agriculture and the Environment, Ames, Iowa, USA.
  • # Contributed equally.
PMID: 25567280 DOI: 10.1038/nature13995
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.

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