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Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides

DOI: 10.1038/s41564-017-0079-1 DOI Help

Authors: Ana S. Luis (Newcastle University) , Jonathon Briggs (Newcastle University) , Xiaoyang Zhang (Newcastle University) , Benjamin Farnell (Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada; University of Lethbridge) , Didier Ndeh (Newcastle University) , Aurore Labourel (Newcastle University) , Arnaud Basle (Newcastle University) , Alan Cartmell (Newcastle University) , Nicolas Terrapon (Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University) , Katherine Stott (University of Cambridge) , Elisabeth C. Lowe (Newcastle University) , Richard Mclean (Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada) , Kaitlyn Shearer (Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada) , Julia Schückel (University of Copenhagen) , Immacolata Venditto (Newcastle University) , Marie-christine Ralet (INRA, UR1268 Biopolymères Interactions Assemblages) , Bernard Henrissat (Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University; INRA, USC 1408 AFMB) , Eric C. Martens (University of Michigan Medical School) , Steven C. Mosimann (University of Lethbridge) , D. Wade Abbott (Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada; University of Lethbridge) , Harry J. Gilbert (Newcastle University)
Co-authored by industrial partner: No

Type: Journal Paper
Journal: Nature Microbiology , VOL 344

State: Published (Approved)
Published: December 2017
Diamond Proposal Number(s): 1960 , 7854 , 9948

Abstract: The major nutrients available to human colonic Bacteroides species are glycans, exemplified by pectins, a network of covalently linked plant cell wall polysaccharides containing galacturonic acid (GalA). Metabolism of complex carbohydrates by the Bacteroides genus is orchestrated by polysaccharide utilization loci (PULs). In Bacteroides thetaiotaomicron, a human colonic bacterium, the PULs activated by different pectin domains have been identified; however, the mechanism by which these loci contribute to the degradation of these GalA-containing polysaccharides is poorly understood. Here we show that each PUL orchestrates the metabolism of specific pectin molecules, recruiting enzymes from two previously unknown glycoside hydrolase families. The apparatus that depolymerizes the backbone of rhamnogalacturonan-I is particularly complex. This system contains several glycoside hydrolases that trim the remnants of other pectin domains attached to rhamnogalacturonan-I, and nine enzymes that contribute to the degradation of the backbone that makes up a rhamnose-GalA repeating unit. The catalytic properties of the pectin-degrading enzymes are optimized to protect the glycan cues that activate the specific PULs ensuring a continuous supply of inducing molecules throughout growth. The contribution of Bacteroides spp. to metabolism of the pectic network is illustrated by cross-feeding between organisms.

Journal Keywords: Bacterial structural biology; Enzymes; Genome informatics; Glycobiology; Microbiome

Subject Areas: Biology and Bio-materials


Instruments: I02-Macromolecular Crystallography , I04-1-Macromolecular Crystallography (fixed wavelength) , I24-Microfocus Macromolecular Crystallography