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      A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes

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          Abstract

          A well-balanced human diet includes a significant intake of non-starch polysaccharides, collectively termed “dietary fibre,” from the cell walls of diverse fruits and vegetables. 1 Due to a paucity of alimentary enzymes encoded by the human genome, 2 our ability to derive energy from dietary fibre depends on saccharification and fermentation of complex carbohydrates by the massive microbial community residing in our distal gut. 3, 4 The xyloglucans (XyGs), in particular, are a ubiquitous family of highly branched plant cell wall polysaccharides 5, 6 whose mechanism(s) of degradation in the human gut and consequent importance in nutrition was heretofore unknown. 1, 7, 8 Here, we demonstrate that a single, complex gene locus in Bacteroides ovatus confers xyloglucan catabolism in this common colonic symbiont. Through targeted gene disruption, biochemical analysis of all predicted glycoside hydrolases and carbohydrate-binding proteins, and three-dimensional structural determination of the vanguard endo-xyloglucanase, we reveal the molecular mechanisms through which XyGs are hydrolysed to component monosaccharides for further metabolism. We also observe that orthologous xyloglucan utilization loci (XyGULs) serve as genetic markers of xyloglucan catabolism in Bacteroidetes, that XyGULs are restricted to a limited number of phylogenetically diverse strains, and that XyGULs are ubiquitous in surveyed human metagenomes. Our findings reveal that the metabolism of even highly abundant components of dietary fibre may be mediated by niche species, which has immediate fundamental and practical implications for gut symbiont population ecology in the context of human diet, nutrition and health. 912

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          Most cited references 35

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          Prediction of lipoprotein signal peptides in Gram-negative bacteria.

          A method to predict lipoprotein signal peptides in Gram-negative Eubacteria, LipoP, has been developed. The hidden Markov model (HMM) was able to distinguish between lipoproteins (SPaseII-cleaved proteins), SPaseI-cleaved proteins, cytoplasmic proteins, and transmembrane proteins. This predictor was able to predict 96.8% of the lipoproteins correctly with only 0.3% false positives in a set of SPaseI-cleaved, cytoplasmic, and transmembrane proteins. The results obtained were significantly better than those of previously developed methods. Even though Gram-positive lipoprotein signal peptides differ from Gram-negatives, the HMM was able to identify 92.9% of the lipoproteins included in a Gram-positive test set. A genome search was carried out for 12 Gram-negative genomes and one Gram-positive genome. The results for Escherichia coli K12 were compared with new experimental data, and the predictions by the HMM agree well with the experimentally verified lipoproteins. A neural network-based predictor was developed for comparison, and it gave very similar results. LipoP is available as a Web server at www.cbs.dtu.dk/services/LipoP/.
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            How glycan metabolism shapes the human gut microbiota.

            Symbiotic microorganisms that reside in the human intestine are adept at foraging glycans and polysaccharides, including those in dietary plants (starch, hemicellulose and pectin), animal-derived cartilage and tissue (glycosaminoglycans and N-linked glycans), and host mucus (O-linked glycans). Fluctuations in the abundance of dietary and endogenous glycans, combined with the immense chemical variation among these molecules, create a dynamic and heterogeneous environment in which gut microorganisms proliferate. In this Review, we describe how glycans shape the composition of the gut microbiota over various periods of time, the mechanisms by which individual microorganisms degrade these glycans, and potential opportunities to intentionally influence this ecosystem for better health and nutrition.
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              Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont.

              The distal human gut is a microbial bioreactor that digests complex carbohydrates. The strategies evolved by gut microbes to sense and process diverse glycans have important implications for the assembly and operation of this ecosystem. The human gut-derived bacterium Bacteroides thetaiotaomicron forages on both host and dietary glycans. Its ability to target these substrates resides in 88 polysaccharide utilization loci (PULs), encompassing 18% of its genome. Whole genome transcriptional profiling and genetic tests were used to define the mechanisms underlying host glycan foraging in vivo and in vitro. PULs that target all major classes of host glycans were identified. However, mucin O-glycans are the principal host substrate foraged in vivo. Simultaneous deletion of five genes encoding ECF-sigma transcription factors, which activate mucin O-glycan utilization, produces defects in bacterial persistence in the gut and in mother-to-offspring transmission. Thus, PUL-mediated glycan catabolism is an important component in gut colonization and may impact microbiota ecology.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                15 December 2014
                19 January 2014
                27 February 2014
                02 January 2015
                : 506
                : 7489
                : 498-502
                Affiliations
                [1 ]Division of Glycoscience, School of Biotechnology, Royal Institute of Technology (KTH), AlbaNova University Centre, 106 91 Stockholm, Sweden
                [2 ]Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI, 48109, USA
                [3 ]Structural Biology Laboratory, Department of Chemistry, University of York, York YO10 5DD, United Kingdom
                [4 ]Wallenberg Wood Science Center, Royal Institute of Technology (KTH), Teknikringen 56-58, 100 44 Stockholm, Sweden
                [5 ]Michael Smith Laboratories and Department of Chemistry, University of British Columbia, 2185 East Mall, Vancouver, BC, V6T 1Z4, Canada
                [6 ]Michael Smith Laboratories and Department of Chemical and Biological Engineering, University of British Columbia, 2185 East Mall, Vancouver, BC, V6T 1Z4, Canada
                Author notes
                Correspondence and requests for materials should be addressed to H.B. ( brumer@ 123456msl.ubc.ca ), E.C.M. ( emartens@ 123456umich.edu ), or G.J.D. ( gideon.davies@ 123456york.ac.uk )
                Article
                NIHMS543896
                10.1038/nature12907
                4282169
                24463512

                Reprints and permissions information is available at www.nature.com/reprints

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