Complex pectin metabolism by gut bacteria reveals novel catalytic functions

Didier Ndeh; Artur Rogowski; Alan Cartmell; Ana S. Luis; Arnaud Baslé; Joseph Gray; Immacolata Venditto; Jonathon Briggs; Xiaoyang Zhang; Aurore Labourel; Nicolas Terrapon; Fanny Buffetto; Sergey Nepogodiev; Yao Xiao; Robert A. Field; Yanping Zhu; Malcolm A. O'Neill; Breeanna R. Urbanowicz; William S. York; Gideon J. Davies; D. Wade Abbott; Marie Christine Ralet; Eric C. Martens; Bernard Henrissat; Harry J. Gilbert

doi:10.1038/nature21725

Complex pectin metabolism by gut bacteria reveals novel catalytic functions

Didier Ndeh, Artur Rogowski, Alan Cartmell, Ana S. Luis, Arnaud Baslé, Joseph Gray, Immacolata Venditto, Jonathon Briggs, Xiaoyang Zhang, Aurore Labourel, Nicolas Terrapon, Fanny Buffetto, Sergey Nepogodiev, Yao Xiao, Robert A. Field, Yanping Zhu, Malcolm A. O'Neill, Breeanna R. Urbanowicz, William S. York, Gideon J. DaviesD. Wade Abbott, Marie Christine Ralet, Eric C. Martens, Bernard Henrissat, Harry J. Gilbert^*

^*Corresponding author for this work

Chemistry

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

Abstract

The metabolism of carbohydrate polymers drives microbial diversity in the human gut microbiota. It is unclear, however, whether bacterial consortia or single organisms are required to depolymerize highly complex glycans. Here we show that the gut bacterium Bacteroides thetaiotaomicron uses the most structurally complex glycan known: The plant pectic polysaccharide rhamnogalacturonan-II, cleaving all but 1 of its 21 distinct glycosidic linkages. The deconstruction of rhamnogalacturonan-II side chains and backbone are coordinated to overcome steric constraints, and the degradation involves previously undiscovered enzyme families and catalytic activities. The degradation system informs revision of the current structural model of rhamnogalacturonan-II and highlights how individual gut bacteria orchestrate manifold enzymes to metabolize the most challenging glycan in the human diet.

Original language	English
Pages (from-to)	65-70
Number of pages	6
Journal	Nature
Volume	544
Issue number	7648
Early online date	22 Mar 2017
DOIs	https://doi.org/10.1038/nature21725
Publication status	Published - 6 Apr 2017

Bibliographical note

© 2017, Macmillan Publishers Limited, part of Springer Nature. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.

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© 2017, Macmillan Publishers Limited, part of Springer Nature. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.
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Ndeh, D., Rogowski, A., Cartmell, A., Luis, A. S., Baslé, A., Gray, J., Venditto, I., Briggs, J., Zhang, X., Labourel, A., Terrapon, N., Buffetto, F., Nepogodiev, S., Xiao, Y., Field, R. A., Zhu, Y., O'Neill, M. A., Urbanowicz, B. R., York, W. S., ... Gilbert, H. J. (2017). Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature, 544(7648), 65-70. https://doi.org/10.1038/nature21725

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abstract = "The metabolism of carbohydrate polymers drives microbial diversity in the human gut microbiota. It is unclear, however, whether bacterial consortia or single organisms are required to depolymerize highly complex glycans. Here we show that the gut bacterium Bacteroides thetaiotaomicron uses the most structurally complex glycan known: The plant pectic polysaccharide rhamnogalacturonan-II, cleaving all but 1 of its 21 distinct glycosidic linkages. The deconstruction of rhamnogalacturonan-II side chains and backbone are coordinated to overcome steric constraints, and the degradation involves previously undiscovered enzyme families and catalytic activities. The degradation system informs revision of the current structural model of rhamnogalacturonan-II and highlights how individual gut bacteria orchestrate manifold enzymes to metabolize the most challenging glycan in the human diet.",

author = "Didier Ndeh and Artur Rogowski and Alan Cartmell and Luis, {Ana S.} and Arnaud Basl{\'e} and Joseph Gray and Immacolata Venditto and Jonathon Briggs and Xiaoyang Zhang and Aurore Labourel and Nicolas Terrapon and Fanny Buffetto and Sergey Nepogodiev and Yao Xiao and Field, {Robert A.} and Yanping Zhu and O'Neill, {Malcolm A.} and Urbanowicz, {Breeanna R.} and York, {William S.} and Davies, {Gideon J.} and Abbott, {D. Wade} and Ralet, {Marie Christine} and Martens, {Eric C.} and Bernard Henrissat and Gilbert, {Harry J.}",

note = "{\textcopyright} 2017, Macmillan Publishers Limited, part of Springer Nature. This is an author-produced version of the published paper. Uploaded in accordance with the publisher{\textquoteright}s self-archiving policy. Further copying may not be permitted; contact the publisher for details.",

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Ndeh, D, Rogowski, A, Cartmell, A, Luis, AS, Baslé, A, Gray, J, Venditto, I, Briggs, J, Zhang, X, Labourel, A, Terrapon, N, Buffetto, F, Nepogodiev, S, Xiao, Y, Field, RA, Zhu, Y, O'Neill, MA, Urbanowicz, BR, York, WS, Davies, GJ, Abbott, DW, Ralet, MC, Martens, EC, Henrissat, B & Gilbert, HJ 2017, 'Complex pectin metabolism by gut bacteria reveals novel catalytic functions', Nature, vol. 544, no. 7648, pp. 65-70. https://doi.org/10.1038/nature21725

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AU - Ndeh, Didier

AU - Rogowski, Artur

AU - Cartmell, Alan

AU - Luis, Ana S.

AU - Baslé, Arnaud

AU - Gray, Joseph

AU - Venditto, Immacolata

AU - Briggs, Jonathon

AU - Zhang, Xiaoyang

AU - Labourel, Aurore

AU - Terrapon, Nicolas

AU - Buffetto, Fanny

AU - Nepogodiev, Sergey

AU - Xiao, Yao

AU - Field, Robert A.

AU - Zhu, Yanping

AU - O'Neill, Malcolm A.

AU - Urbanowicz, Breeanna R.

AU - York, William S.

AU - Davies, Gideon J.

AU - Abbott, D. Wade

AU - Ralet, Marie Christine

AU - Martens, Eric C.

AU - Henrissat, Bernard

AU - Gilbert, Harry J.

N1 - © 2017, Macmillan Publishers Limited, part of Springer Nature. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details.

PY - 2017/4/6

Y1 - 2017/4/6

N2 - The metabolism of carbohydrate polymers drives microbial diversity in the human gut microbiota. It is unclear, however, whether bacterial consortia or single organisms are required to depolymerize highly complex glycans. Here we show that the gut bacterium Bacteroides thetaiotaomicron uses the most structurally complex glycan known: The plant pectic polysaccharide rhamnogalacturonan-II, cleaving all but 1 of its 21 distinct glycosidic linkages. The deconstruction of rhamnogalacturonan-II side chains and backbone are coordinated to overcome steric constraints, and the degradation involves previously undiscovered enzyme families and catalytic activities. The degradation system informs revision of the current structural model of rhamnogalacturonan-II and highlights how individual gut bacteria orchestrate manifold enzymes to metabolize the most challenging glycan in the human diet.

AB - The metabolism of carbohydrate polymers drives microbial diversity in the human gut microbiota. It is unclear, however, whether bacterial consortia or single organisms are required to depolymerize highly complex glycans. Here we show that the gut bacterium Bacteroides thetaiotaomicron uses the most structurally complex glycan known: The plant pectic polysaccharide rhamnogalacturonan-II, cleaving all but 1 of its 21 distinct glycosidic linkages. The deconstruction of rhamnogalacturonan-II side chains and backbone are coordinated to overcome steric constraints, and the degradation involves previously undiscovered enzyme families and catalytic activities. The degradation system informs revision of the current structural model of rhamnogalacturonan-II and highlights how individual gut bacteria orchestrate manifold enzymes to metabolize the most challenging glycan in the human diet.

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VL - 544

SP - 65

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JO - Nature

JF - Nature

IS - 7648

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Complex pectin metabolism by gut bacteria reveals novel catalytic functions

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Gideon John Davies, FRS, FMedSci

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Complex pectin metabolism by gut bacteria reveals novel catalytic functions

Abstract

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Gideon John Davies, FRS, FMedSci

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