Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

• Published in: Nature (London) 2015-01, Vol.517 (7533), p.165-169
• Main Authors: Cuskin, Fiona, Lowe, Elisabeth C., Temple, Max J., Zhu, Yanping, Cameron, Elizabeth A., Pudlo, Nicholas A., Porter, Nathan T., Urs, Karthik, Thompson, Andrew J., Cartmell, Alan, Rogowski, Artur, Hamilton, Brian S., Chen, Rui, Tolbert, Thomas J., Piens, Kathleen, Bracke, Debby, Vervecken, Wouter, Hakki, Zalihe, Speciale, Gaetano, Munōz-Munōz, Jose L., Day, Andrew, Peña, Maria J., McLean, Richard, Suits, Michael D., Boraston, Alisdair B., Atherly, Todd, Ziemer, Cherie J., Williams, Spencer J., Davies, Gideon J., Abbott, D. Wade, Martens, Eric C., Gilbert, Harry J.
• Format: Article
• Language: English
• Subjects: 45; 631/326; 82; 82/83; Animals; Bacteria; Bacteroidetes - cytology; Bacteroidetes - enzymology; Bacteroidetes - genetics; Bacteroidetes - metabolism; BASIC BIOLOGICAL SCIENCES; Biochemical analysis; Biological Evolution; Carbohydrate Conformation; Diet; Digestive system; Enzymes; Enzymes - genetics; Enzymes - metabolism; Female; Gastrointestinal Tract - microbiology; Genetic Loci - genetics; Genomes; Germ-Free Life; Glycoproteins - chemistry; Glycoproteins - metabolism; Humanities and Social Sciences; Humans; Male; Mannans - chemistry; Mannans - metabolism; Mannose - metabolism; Metabolism; Mice; Microbiology; Microorganisms; Models, Biological; Models, Molecular; multidisciplinary; Oligosaccharides - chemistry; Oligosaccharides - metabolism; Periplasm - enzymology; Science; Science & Technology - Other Topics; Yeast; Yeasts; Yeasts - chemistry
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature13995

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. Mannan, a component of yeast cell walls, is shown to be a viable food source for Bacteroides thetaiotamicron , a dominant member of the gut microbiota, which catabolizes the mannan ‘selfishly’—countering the general assumption that multiple members of the gut microbiota take a role in, and benefit from, polysaccharide catabolism. A gut microbe with a taste for yeast Harry Gilbert and colleagues show that Bacteroides thetaiotaomicron , a dominant member of the human gut microbiota, can utilize α-mannose-containing complex carbohydrates derived from both host glycoproteins and yeast-derived dietary polysaccharides as a viable food source. The authors identify the genetic loci that encode the machinery that allows B. thetaiotamicron to metabolize α-mannan via large oligosaccharides that are subsequently depolymerized to mannose by the action of periplasmic enzymes. Co-culturing studies reveal a 'selfish' model for α-mannan catabolism, which runs counter to the general assumption that multiple members of the gut microbiota take a role in, and benefit from, polysaccharide catabolism. This study provides insight into how the evolution of glycan degradation in the human gut microbiota mirrors dietary changes during the course of human evolution, as yeast α-mannan has become a ubiquitous dietary component of our diet only since the acquisition of the modern human diet.