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ARS Home » Midwest Area » Ames, Iowa » National Laboratory for Agriculture and The Environment » Agroecosystems Management Research » Research » Publications at this Location » Publication #303841
Title: Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Author
item CUSKIN, FIONA - Newcastle University
item LOWE, ELISABETH - Newcastle University
item TEMPLE, MAX - Newcastle University
item ZHU, YANPING - Newcastle University
item CAMERON, ELIZABETH - University Of Michigan Medical School
item PUDLO, NICHOLAS - University Of Michigan Medical School
item PORTER, NATHAN - University Of Michigan Medical School
item URS, KARTHIK - University Of Michigan Medical School
item THOMPSON, ANDREW - University Of York
item CARTMELL, ALAN - University Of Melbourne
item ROGOWSKI, ARTHUR - Newcastle University
item HAMILTON, BRIAN - Indiana University
item CHEN, RUI - Indiana University
item TOLBERT, THOMAS - University Of Kansas Medical School
item PIENS, KATHLEEN - Oxyrane
item BRACKE, DEBBY - Oxyrane
item VERVECKEN, WOUTER - Oxyrane
item HAKKI, ZALIHE - University Of Melbourne
item SPECIALE, GAETANO - Melbourne University
item MUNOZ-MUNOZ, JOSE - Newcastle University
item DAY, ANDREW - Newcastle University
item PENA, MARIA - University Of Georgia
item MCLEAN, RICHARD - Agriculture And Agri-Food Canada
item SUITS, MICHAEL - University Of Victoria
item BORASTON, ALISDAIR - University Of Victoria
item Atherly, Todd
item Ziemer, Cherie
item WILLIAMS, SPENCER - University Of Melbourne
item DAVIES, GIDEON - University Of York
item ABBOTT, WADE - University Of Georgia
item MARTENS, ERIC - University Of Michigan Medical School
item GILBERT, HARRY - Newcastle University

Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/25/2014
Publication Date: 1/8/2015
Citation: Cuskin, F., Lowe, E., Temple, M., Zhu, Y., Cameron, E.A., Pudlo, N., Porter, N.T., Urs, K., Thompson, A., Cartmell, A., Rogowski, A., Hamilton, B.S., Chen, R., Tolbert, T., Piens, K., Bracke, D., Vervecken, W., Hakki, Z., Speciale, G., Munoz-Munoz, J., Day, A., Pena, M., McLean, R., Suits, M., Boraston, A., Atherly, T.A., Ziemer, C.J., Williams, S., Davies, G., Abbott, W., Martens, E., Gilbert, H. 2015. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature. 517:165-169. DOI: 10.1038/nature13995.

Interpretive Summary: The human diet contains many complex carbohydrates which cannot be utilized without enzymes produced by gut microbes. Yeasts and other fungi have some complex carbohydrates such as mannan which are not found in plants. Yeasts are some of the earliest 'domesticated' microbes and have been part of the human diet for at least 7000 years. The gut bacterium Bacteroides thetaioataomicron, a predominant gut microbe, contains a number of genes capable of degrading mannan; these genes are not found in many gut bacteria. These data support a 'selfish' model of carbohydrate utilization, as apposed to a 'sharing' model, a currently held hypothesis which suggests extensive synergy amongst gut bacteria for utilization of complex carbohydrates. Bacteroides thetaiotaomicron has evolved the specific and somewhat unique ability to utilize yeast carbohydrates. This demonstrates an important linkage between gut microbes and human nutrition as well as adaptive gut bacterial evolution in response to human dietary changes. Both humans and animals will beneift from the understanding gained from studying these intestinal bacteria and their effects in health and disease.

Technical Abstract: The architecture of the human distal gut microbiota (microbiota) is sculpted by the complex carbohydrates delivered in the diet. Yeasts, which are among the earliest domesticated microorganisms and have been a component of the human diet for at least 7000 years, possess an elaborate cell wall alpha-mannan. The influence of yeast mannan on the ecology of the microbiota, however, is unknown. Significantly, Bacteroides thetaiotaomicron (Bt), a dominant and widespread member of the human large bowel microbial community, has a genome that encodes an extensive repertoire of enzymes capable of hydrolyzing alpha-mannosidic linkages. We show here using transcriptional analysis, enzyme specificity, cellular localization, structural biology, chromosomal modifications and gnotobiotic mouse experiments that yeast alpha-mannan is a viable food source for Bt. Furthermore, distinct polysaccharide utilization loci (PULs) orchestrate the differential degradation of yeast alpha-mannan and high mannose mammalian N-glycans (HMNGs) in spite of their structural similarities. We propose a model whereby limited cleavage of the alpha-mannan backbone by surface endo-alpha1,6-mannanases generates large oligosaccharides that are depolymerized to mannose by the synergistic action of an array of specific periplasmic exo- and endo-acting glycoside hydrolases and phosphatases. The metabolism of yeast mannan by Bt supports a 'selfish' model for polysaccharide catabolism at odds with the 'nutrient sharing' hypothesis that suggests extensive synergy between members of the microbiota in the utilization of complex carbohydrates. This report shows how a cohort of highly successful members of the microbiota have evolved to consume sterically-restricted glycans presented on the surface of yeasts, an adaptation to the domestication of yeast and its increasing impact on the civilized human diet.