Complex pectin metabolism by gut bacteria reveals novel catalytic functions

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.

doi:10.1038/nature21725

Title: Complex pectin metabolism by gut bacteria reveals novel catalytic functions

Journal Article · Thu Apr 06 00:00:00 EDT 2017 · Nature (London)

DOI:https://doi.org/10.1038/nature21725· OSTI ID:1473846

Ndeh, Didier ^[1]; Rogowski, Artur ^[1]; Cartmell, Alan ^[1]; Luis, Ana S. ^[1]; Baslé, Arnaud ^[1]; Gray, Joseph ^[1]; Venditto, Immacolata ^[1]; Briggs, Jonathon ^[1]; Zhang, Xiaoyang ^[1]; Labourel, Aurore ^[1]; Terrapon, Nicolas ^[2]; Buffetto, Fanny ^[3]; Nepogodiev, Sergey ^[4]; Xiao, Yao ^[5]; Field, Robert A. ^[4]; Zhu, Yanping ^[6]; O’Neill, Malcolm A. ^[6]; Urbanowicz, Breeanna R. ^[6]; York, William S. ^[6]; Davies, Gideon J. ^[7] more »

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

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.

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Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-12ER16324; SC0008472

OSTI ID:: 1473846

Journal Information:: Nature (London), Vol. 544, Issue 7648; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 360 works

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MUR1‐mediated cell‐wall fucosylation is required for freezing tolerance in Arabidopsis thaliana Panter, Paige E.; Kent, Olivia; Dale, Maeve New Phytologist, Vol. 224, Issue 4 https://doi.org/10.1111/nph.16209	journal	September 2019
Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II Sechet, Julien; Htwe, Soe; Urbanowicz, Breeanna The Plant Journal, Vol. 96, Issue 5 https://doi.org/10.1111/tpj.14088	journal	October 2018
Locating Methyl-Etherified and Methyl-Esterified Uronic Acids in the Plant Cell Wall Pectic Polysaccharide Rhamnogalacturonan II O’Neill, Malcolm A.; Black, Ian; Urbanowicz, Breeanna SLAS TECHNOLOGY: Translating Life Sciences Innovation, Vol. 25, Issue 4 https://doi.org/10.1177/2472630320923321	journal	May 2020
A novel acetyl xylan esterase enabling complete deacetylation of substituted xylans Razeq, Fakhria M.; Jurak, Edita; Stogios, Peter J. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1074-3	journal	March 2018
Multimodular fused acetyl–feruloyl esterases from soil and gut Bacteroidetes improve xylanase depolymerization of recalcitrant biomass Kmezik, Cathleen; Bonzom, Cyrielle; Olsson, Lisbeth Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01698-9	journal	March 2020
Competitive lottery-based assembly of selected clades in the human gut microbiome Verster, Adrian J.; Borenstein, Elhanan Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0571-8	journal	October 2018
Specificity and mechanism of carbohydrate demethylation by cytochrome P450 monooxygenases Robb, Craig S.; Reisky, Lukas; Bornscheuer, Uwe T. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-00025	text	January 2018
Gene Expression Analysis of Zobellia galactanivorans during the Degradation of Algal Polysaccharides Reveals both Substrate-Specific and Shared Transcriptome-Wide Responses Thomas, François; Bordron, Philippe; Eveillard, Damien Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01808	journal	September 2017
Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02340	journal	December 2017
Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression Amos, Robert A.; Mohnen, Debra Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00915	journal	July 2019
Systematic Review of Gut Microbiota and Major Depression Cheung, Stephanie G.; Goldenthal, Ariel R.; Uhlemann, Anne-Catrin Frontiers in Psychiatry, Vol. 10 https://doi.org/10.3389/fpsyt.2019.00034	journal	February 2019
Synthesis of Two Tetrasaccharide Pentenyl Glycosides Related to the Pectic Rhamnogalacturonan I Polysaccharide Zakharova, Alexandra; Awan, Shahid; Nami, Faranak Molecules, Vol. 23, Issue 2 https://doi.org/10.3390/molecules23020327	journal	February 2018
Towards an Integrative Understanding of tRNA Aminoacylation–Diet–Host–Gut Microbiome Interactions in Neurodegeneration Paley, Elena; Perry, George Nutrients, Vol. 10, Issue 4 https://doi.org/10.3390/nu10040410	journal	March 2018
High‐Throughput Approaches in Carbohydrate‐Active Enzymology: Glycosidase and Glycosyl Transferase Inhibitors, Evolution, and Discovery Chao, Lemeng; Jongkees, Seino Angewandte Chemie, Vol. 131, Issue 37 https://doi.org/10.1002/ange.201900055	journal	July 2019
Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria Ficko-Blean, Elizabeth; Préchoux, Aurélie; Thomas, François Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01832-6	journal	November 2017
Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont Pluvinage, Benjamin; Grondin, Julie M.; Amundsen, Carolyn Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03366-x	journal	March 2018
Identification of endoxylanase XynE from Clostridium thermocellum as the first xylanase of glycoside hydrolase family GH141 Heinze, Simon; Mechelke, Matthias; Kornberger, Petra Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-11598-y	journal	September 2017
Unusual active site location and catalytic apparatus in a glycoside hydrolase family Munoz-Munoz, Jose; Cartmell, Alan; Terrapon, Nicolas Proceedings of the National Academy of Sciences, Vol. 114, Issue 19 https://doi.org/10.1073/pnas.1701130114	journal	April 2017
PULDB: the expanded database of Polysaccharide Utilization Loci Terrapon, Nicolas; Lombard, Vincent; Drula, Élodie Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1022	journal	October 2017
Ten years of CAZypedia : A living encyclopedia of carbohydrate-active enzymes Consortium, The CAZypedia The University of British Columbia https://doi.org/10.14288/1.0357263	text	January 2018
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Luis, Ana S.; Briggs, Jonathon; Zhang, Xiaoyang Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.27636	text	January 2018
Adaptive mechanisms that provide competitive advantages to marine bacteroidetes during microalgal blooms Unfried, Frank; Becker, Stefan; Robb, Craig S. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-00030	text	January 2018
Gut Fermentation of Dietary Fibres: Physico-Chemistry of Plant Cell Walls and Implications for Health Williams, Barbara; Grant, Lucas; Gidley, Michael International Journal of Molecular Sciences, Vol. 18, Issue 10 https://doi.org/10.3390/ijms18102203	journal	October 2017
Precision Nutrition and the Microbiome, Part I: Current State of the Science Mills, Susan; Stanton, Catherine; Lane, Jonathan Nutrients, Vol. 11, Issue 4 https://doi.org/10.3390/nu11040923	journal	April 2019
Specificity and mechanism of carbohydrate demethylation by cytochrome P450 monooxygenases Robb, Craig S.; Reisky, Lukas; Bornscheuer, Uwe T. Biochemical Journal, Vol. 475, Issue 23 https://doi.org/10.1042/bcj20180762	journal	December 2018
A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment Li, Junhua; Zhong, Huanzi; Ramayo-Caldas, Yuliaxis GigaScience, Vol. 9, Issue 6 https://doi.org/10.1093/gigascience/giaa057	journal	May 2020
Single cell fluorescence imaging of glycan uptake by intestinal bacteria Hehemann, Jan-Hendrik; Reintjes, Greta; Klassen, Leeann Zenodo https://doi.org/10.5281/zenodo.5517311	journalarticle	January 2019
Single cell fluorescence imaging of glycan uptake by intestinal bacteria Hehemann, Jan-Hendrik; Reintjes, Greta; Klassen, Leeann Zenodo https://doi.org/10.5281/zenodo.5517312	journalarticle	January 2019

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