Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Fiona Cuskin; Elisabeth C Lowe; Max J Temple; Yanping Zhu; Elizabeth Cameron; Nicholas A Pudlo; Nathan T Porter; Karthik Urs; Andrew J 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 D Suits; Alisdair B Boraston; Todd Atherly; Cherie J Ziemer; Spencer J Williams; Gideon J 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 Cameron, Nicholas A Pudlo, Nathan T Porter, Karthik Urs, Andrew J 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 D Suits, Alisdair B Boraston, Todd Atherly, Cherie J Ziemer, Spencer J Williams, Gideon J Davies, D Wade Abbott, Eric C Martens, Harry J Gilbert

Applied Sciences Department

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402 Citations (Scopus)

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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

Keywords

Animals
Bacteroidetes/cytology
Biological Evolution
Carbohydrate Conformation
Diet
Enzymes/genetics
Female
Gastrointestinal Tract/microbiology
Genetic Loci/genetics
Germ-Free Life
Glycoproteins/chemistry
Humans
Male
Mannans/chemistry
Mannose/metabolism
Mice
Models, Biological
Models, Molecular
Oligosaccharides/chemistry
Periplasm/enzymology
Yeasts/chemistry

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10.1038/nature13995

Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanismAccepted author manuscript, 9.63 MB

https://eprint.ncl.ac.uk/210624Licence: CC BY-NC

Cite this

Cuskin, F., Lowe, E. C., Temple, M. J., Zhu, Y., Cameron, E., 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

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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. ",

keywords = "Animals, Bacteroidetes/cytology, Biological Evolution, Carbohydrate Conformation, Diet, Enzymes/genetics, Female, Gastrointestinal Tract/microbiology, Genetic Loci/genetics, Germ-Free Life, Glycoproteins/chemistry, Humans, Male, Mannans/chemistry, Mannose/metabolism, Mice, Models, Biological, Models, Molecular, Oligosaccharides/chemistry, Periplasm/enzymology, Yeasts/chemistry",

author = "Fiona Cuskin and Lowe, {Elisabeth C} and Temple, {Max J} and Yanping Zhu and Elizabeth Cameron and Pudlo, {Nicholas A} and Porter, {Nathan T} and Karthik Urs and Thompson, {Andrew J} 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 D} and Boraston, {Alisdair B} and Todd Atherly and Ziemer, {Cherie J} and Williams, {Spencer J} and Davies, {Gideon J} 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",

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Cuskin, F, Lowe, EC, Temple, MJ, Zhu, Y, Cameron, E, 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, MD, 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

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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

AU - Pudlo, Nicholas A

AU - Porter, Nathan T

AU - Urs, Karthik

AU - Thompson, Andrew J

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 D

AU - Boraston, Alisdair B

AU - Atherly, Todd

AU - Ziemer, Cherie J

AU - Williams, Spencer J

AU - Davies, Gideon J

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.

KW - Animals

KW - Bacteroidetes/cytology

KW - Biological Evolution

KW - Carbohydrate Conformation

KW - Diet

KW - Enzymes/genetics

KW - Female

KW - Gastrointestinal Tract/microbiology

KW - Genetic Loci/genetics

KW - Germ-Free Life

KW - Glycoproteins/chemistry

KW - Humans

KW - Male

KW - Mannans/chemistry

KW - Mannose/metabolism

KW - Mice

KW - Models, Biological

KW - Models, Molecular

KW - Oligosaccharides/chemistry

KW - Periplasm/enzymology

KW - Yeasts/chemistry

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

Keywords

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