Complex pectin metabolism by gut bacteria reveals novel catalytic functions
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 in this paper 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.
- Authors:
-
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- Newcastle Univ., Newcastle upon Tyne (United Kingdom). Inst. for Cell and Molecular Biosciences
- Centre National de la Recherche Scientifique (CNRS), Marseille (France). Architecture et Fonction des Macromolécules Biologiques; Aix-Marseille Univ., Marseille (France)
- INRA, Nantes (France). Biopolymères Interactions Assemblages
- John Innes Centre Norwich Research Park, Norwich (United Kingdom). Dept. of Biological Chemistry
- Univ. of Michigan, Ann Arbor, MI (United States). Medical School, Dept. of Microbiology and Immunology
- Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
- Univ. of York (United Kingdom). Dept. of Chemistry
- Lethbridge Research Centre, Lethbridge, AB (Canada)
- Centre National de la Recherche Scientifique (CNRS), Marseille (France). Architecture et Fonction des Macromolécules Biologiques; Aix-Marseille Univ., Marseille (France); INRA, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia). Dept. of Biological Sciences
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1473846
- Grant/Contract Number:
- FG02-12ER16324; SC0008472
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 544; Journal Issue: 7648; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Ndeh, Didier, Rogowski, Artur, Cartmell, Alan, Luis, Ana S., Baslé, Arnaud, Gray, Joseph, Venditto, Immacolata, Briggs, Jonathon, Zhang, Xiaoyang, Labourel, Aurore, Terrapon, Nicolas, Buffetto, Fanny, Nepogodiev, Sergey, Xiao, Yao, Field, Robert A., Zhu, Yanping, O’Neill, Malcolm A., Urbanowicz, Breeanna R., York, William S., Davies, Gideon J., Abbott, D. Wade, Ralet, Marie-Christine, Martens, Eric C., Henrissat, Bernard, and Gilbert, Harry J. Complex pectin metabolism by gut bacteria reveals novel catalytic functions. United States: N. p., 2017.
Web. doi:10.1038/nature21725.
Ndeh, Didier, Rogowski, Artur, Cartmell, Alan, Luis, Ana S., Baslé, Arnaud, Gray, Joseph, Venditto, Immacolata, Briggs, Jonathon, Zhang, Xiaoyang, Labourel, Aurore, Terrapon, Nicolas, Buffetto, Fanny, Nepogodiev, Sergey, Xiao, Yao, Field, Robert A., Zhu, Yanping, O’Neill, Malcolm A., Urbanowicz, Breeanna R., York, William S., Davies, Gideon J., Abbott, D. Wade, Ralet, Marie-Christine, Martens, Eric C., Henrissat, Bernard, & Gilbert, Harry J. Complex pectin metabolism by gut bacteria reveals novel catalytic functions. United States. https://doi.org/10.1038/nature21725
Ndeh, Didier, Rogowski, Artur, Cartmell, Alan, Luis, Ana S., Baslé, Arnaud, Gray, Joseph, Venditto, Immacolata, Briggs, Jonathon, Zhang, Xiaoyang, Labourel, Aurore, Terrapon, Nicolas, Buffetto, Fanny, Nepogodiev, Sergey, Xiao, Yao, Field, Robert A., Zhu, Yanping, O’Neill, Malcolm A., Urbanowicz, Breeanna R., York, William S., Davies, Gideon J., Abbott, D. Wade, Ralet, Marie-Christine, Martens, Eric C., Henrissat, Bernard, and Gilbert, Harry J. Thu .
"Complex pectin metabolism by gut bacteria reveals novel catalytic functions". United States. https://doi.org/10.1038/nature21725. https://www.osti.gov/servlets/purl/1473846.
@article{osti_1473846,
title = {Complex pectin metabolism by gut bacteria reveals novel catalytic functions},
author = {Ndeh, Didier and Rogowski, Artur and Cartmell, Alan and Luis, Ana S. and Baslé, Arnaud and Gray, Joseph and Venditto, Immacolata and Briggs, Jonathon and Zhang, Xiaoyang and Labourel, Aurore and Terrapon, Nicolas and Buffetto, Fanny and Nepogodiev, Sergey and Xiao, Yao and Field, Robert A. and Zhu, Yanping 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 Henrissat, Bernard and Gilbert, Harry J.},
abstractNote = {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 in this paper 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.},
doi = {10.1038/nature21725},
journal = {Nature (London)},
number = 7648,
volume = 544,
place = {United States},
year = {Thu Apr 06 00:00:00 EDT 2017},
month = {Thu Apr 06 00:00:00 EDT 2017}
}
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- Razeq, Fakhria M.; Jurak, Edita; Stogios, Peter J.
- Biotechnology for Biofuels, Vol. 11, Issue 1
Multimodular fused acetyl–feruloyl esterases from soil and gut Bacteroidetes improve xylanase depolymerization of recalcitrant biomass
journal, March 2020
- Kmezik, Cathleen; Bonzom, Cyrielle; Olsson, Lisbeth
- Biotechnology for Biofuels, Vol. 13, Issue 1
Competitive lottery-based assembly of selected clades in the human gut microbiome
journal, October 2018
- Verster, Adrian J.; Borenstein, Elhanan
- Microbiome, Vol. 6, Issue 1
Specificity and mechanism of carbohydrate demethylation by cytochrome P450 monooxygenases
text, January 2018
- Robb, Craig S.; Reisky, Lukas; Bornscheuer, Uwe T.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Gene Expression Analysis of Zobellia galactanivorans during the Degradation of Algal Polysaccharides Reveals both Substrate-Specific and Shared Transcriptome-Wide Responses
journal, September 2017
- Thomas, François; Bordron, Philippe; Eveillard, Damien
- Frontiers in Microbiology, Vol. 8
Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria
journal, December 2017
- Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric
- Frontiers in Microbiology, Vol. 8
Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression
journal, July 2019
- Amos, Robert A.; Mohnen, Debra
- Frontiers in Plant Science, Vol. 10
Systematic Review of Gut Microbiota and Major Depression
journal, February 2019
- Cheung, Stephanie G.; Goldenthal, Ariel R.; Uhlemann, Anne-Catrin
- Frontiers in Psychiatry, Vol. 10
Synthesis of Two Tetrasaccharide Pentenyl Glycosides Related to the Pectic Rhamnogalacturonan I Polysaccharide
journal, February 2018
- Zakharova, Alexandra; Awan, Shahid; Nami, Faranak
- Molecules, Vol. 23, Issue 2
Towards an Integrative Understanding of tRNA Aminoacylation–Diet–Host–Gut Microbiome Interactions in Neurodegeneration
journal, March 2018
- Paley, Elena; Perry, George
- Nutrients, Vol. 10, Issue 4
High‐Throughput Approaches in Carbohydrate‐Active Enzymology: Glycosidase and Glycosyl Transferase Inhibitors, Evolution, and Discovery
journal, July 2019
- Chao, Lemeng; Jongkees, Seino
- Angewandte Chemie, Vol. 131, Issue 37
Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria
journal, November 2017
- Ficko-Blean, Elizabeth; Préchoux, Aurélie; Thomas, François
- Nature Communications, Vol. 8, Issue 1
Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont
journal, March 2018
- Pluvinage, Benjamin; Grondin, Julie M.; Amundsen, Carolyn
- Nature Communications, Vol. 9, Issue 1
Identification of endoxylanase XynE from Clostridium thermocellum as the first xylanase of glycoside hydrolase family GH141
journal, September 2017
- Heinze, Simon; Mechelke, Matthias; Kornberger, Petra
- Scientific Reports, Vol. 7, Issue 1
Unusual active site location and catalytic apparatus in a glycoside hydrolase family
journal, April 2017
- Munoz-Munoz, Jose; Cartmell, Alan; Terrapon, Nicolas
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 19
PULDB: the expanded database of Polysaccharide Utilization Loci
journal, October 2017
- Terrapon, Nicolas; Lombard, Vincent; Drula, Élodie
- Nucleic Acids Research, Vol. 46, Issue D1
Ten years of CAZypedia : A living encyclopedia of carbohydrate-active enzymes
text, January 2018
- Consortium, The CAZypedia
- The University of British Columbia
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides.
text, January 2018
- Luis, Ana S.; Briggs, Jonathon; Zhang, Xiaoyang
- Apollo - University of Cambridge Repository
Adaptive mechanisms that provide competitive advantages to marine bacteroidetes during microalgal blooms
text, January 2018
- Unfried, Frank; Becker, Stefan; Robb, Craig S.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Gut Fermentation of Dietary Fibres: Physico-Chemistry of Plant Cell Walls and Implications for Health
journal, October 2017
- Williams, Barbara; Grant, Lucas; Gidley, Michael
- International Journal of Molecular Sciences, Vol. 18, Issue 10
Precision Nutrition and the Microbiome, Part I: Current State of the Science
journal, April 2019
- Mills, Susan; Stanton, Catherine; Lane, Jonathan
- Nutrients, Vol. 11, Issue 4
Specificity and mechanism of carbohydrate demethylation by cytochrome P450 monooxygenases
journal, December 2018
- Robb, Craig S.; Reisky, Lukas; Bornscheuer, Uwe T.
- Biochemical Journal, Vol. 475, Issue 23
A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
journal, May 2020
- Li, Junhua; Zhong, Huanzi; Ramayo-Caldas, Yuliaxis
- GigaScience, Vol. 9, Issue 6
Single cell fluorescence imaging of glycan uptake by intestinal bacteria
journalarticle, January 2019
- Hehemann, Jan-Hendrik; Reintjes, Greta; Klassen, Leeann
- Zenodo
Single cell fluorescence imaging of glycan uptake by intestinal bacteria
journalarticle, January 2019
- Hehemann, Jan-Hendrik; Reintjes, Greta; Klassen, Leeann
- Zenodo