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

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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

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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

@article{f05561147f4a49f6a203fe33f96219d5,

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",

pages = "165--169",

journal = "Nature",

issn = "0028-0836",

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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

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

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

UR - https://www.scopus.com/pages/publications/84922629682

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

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