Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Fiona Cuskin; Elisabeth C Lowe; Max J Temple; Yanping Zhu; Elizabeth A Cameron; Nicholas A Pudlo; Nathan T Porter; Karthik Urs; Andrew James Thompson; Alan Cartmell; Artur Rogowski; Brian S Hamilton; Rui Chen; Thomas J Tolbert; Kathleen Piens; Debby Bracke; Wouter Vervecken; Zalihe Hakki; Gaetano Speciale; Jose L Munōz-Munōz; Andrew Day; Maria J Peña; Richard McLean; Michael Douglas Leo Suits; Alisdair B Boraston; Todd Atherly; Cherie J Ziemer; Spencer J Williams; Gideon John Davies; D Wade Abbott; Eric C Martens; Harry J Gilbert

doi:10.1038/nature13995

Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Fiona Cuskin, Elisabeth C Lowe, Max J Temple, Yanping Zhu, Elizabeth A Cameron, Nicholas A Pudlo, Nathan T Porter, Karthik Urs, Andrew James Thompson, Alan Cartmell, Artur Rogowski, Brian S Hamilton, Rui Chen, Thomas J Tolbert, Kathleen Piens, Debby Bracke, Wouter Vervecken, Zalihe Hakki, Gaetano Speciale, Jose L Munōz-MunōzAndrew Day, Maria J Peña, Richard McLean, Michael Douglas Leo Suits, Alisdair B Boraston, Todd Atherly, Cherie J Ziemer, Spencer J Williams, Gideon John Davies, D Wade Abbott, Eric C Martens, Harry J Gilbert

Chemistry

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Pages (from-to)	165-169
Number of pages	5
Journal	Nature
Volume	517
Issue number	7533
Early online date	7 Jan 2015
DOIs	https://doi.org/10.1038/nature13995
Publication status	Published - 8 Jan 2015

Access to Document

10.1038/nature13995

Gideon John Davies, FRS, FMedSci
- gideon.daviesyork.acuk
- Chemistry - Professor
Person: Academic

Cite this

Cuskin, F., Lowe, E. C., Temple, M. J., Zhu, Y., Cameron, E. A., Pudlo, N. A., Porter, N. T., Urs, K., Thompson, A. J., Cartmell, A., Rogowski, A., Hamilton, B. S., Chen, R., Tolbert, T. J., Piens, K., Bracke, D., Vervecken, W., Hakki, Z., Speciale, G., ... Gilbert, H. J. (2015). Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature, 517(7533), 165-169. https://doi.org/10.1038/nature13995

@article{a9fd6febe81b42a397901d4ab9f4afa3,

title = "Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism",

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.",

author = "Fiona Cuskin and Lowe, {Elisabeth C} and Temple, {Max J} and Yanping Zhu and Cameron, {Elizabeth A} and Pudlo, {Nicholas A} and Porter, {Nathan T} and Karthik Urs and Thompson, {Andrew James} and Alan Cartmell and Artur Rogowski and Hamilton, {Brian S} and Rui Chen and Tolbert, {Thomas J} and Kathleen Piens and Debby Bracke and Wouter Vervecken and Zalihe Hakki and Gaetano Speciale and Munōz-Munōz, {Jose L} and Andrew Day and Pe{\~n}a, {Maria J} and Richard McLean and Suits, {Michael Douglas Leo} and Boraston, {Alisdair B} and Todd Atherly and Ziemer, {Cherie J} and Williams, {Spencer J} and Davies, {Gideon John} and Abbott, {D Wade} and Martens, {Eric C} and Gilbert, {Harry J}",

year = "2015",

month = jan,

day = "8",

doi = "10.1038/nature13995",

language = "English",

volume = "517",

pages = "165--169",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7533",

}

Cuskin, F, Lowe, EC, Temple, MJ, Zhu, Y, Cameron, EA, Pudlo, NA, Porter, NT, Urs, K, Thompson, AJ, Cartmell, A, Rogowski, A, Hamilton, BS, Chen, R, Tolbert, TJ, Piens, K, Bracke, D, Vervecken, W, Hakki, Z, Speciale, G, Munōz-Munōz, JL, Day, A, Peña, MJ, McLean, R, Suits, MDL, Boraston, AB, Atherly, T, Ziemer, CJ, Williams, SJ, Davies, GJ, Abbott, DW, Martens, EC & Gilbert, HJ 2015, 'Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism', Nature, vol. 517, no. 7533, pp. 165-169. https://doi.org/10.1038/nature13995

TY - JOUR

T1 - Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

AU - Cuskin, Fiona

AU - Lowe, Elisabeth C

AU - Temple, Max J

AU - Zhu, Yanping

AU - Cameron, Elizabeth A

AU - Pudlo, Nicholas A

AU - Porter, Nathan T

AU - Urs, Karthik

AU - Thompson, Andrew James

AU - Cartmell, Alan

AU - Rogowski, Artur

AU - Hamilton, Brian S

AU - Chen, Rui

AU - Tolbert, Thomas J

AU - Piens, Kathleen

AU - Bracke, Debby

AU - Vervecken, Wouter

AU - Hakki, Zalihe

AU - Speciale, Gaetano

AU - Munōz-Munōz, Jose L

AU - Day, Andrew

AU - Peña, Maria J

AU - McLean, Richard

AU - Suits, Michael Douglas Leo

AU - Boraston, Alisdair B

AU - Atherly, Todd

AU - Ziemer, Cherie J

AU - Williams, Spencer J

AU - Davies, Gideon John

AU - Abbott, D Wade

AU - Martens, Eric C

AU - Gilbert, Harry J

PY - 2015/1/8

Y1 - 2015/1/8

N2 - 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.

AB - 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.

U2 - 10.1038/nature13995

DO - 10.1038/nature13995

M3 - Article

C2 - 25567280

SN - 0028-0836

VL - 517

SP - 165

EP - 169

JO - Nature

JF - Nature

IS - 7533

ER -

Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Abstract

Access to Document

Profiles

Gideon John Davies, FRS, FMedSci

Cite this