Publication Date:
2014-01-28
Description:
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. Owing to the paucity of alimentary enzymes encoded by the human genome, our ability to derive energy from dietary fibre depends on the saccharification and fermentation of complex carbohydrates by the massive microbial community residing in our distal gut. The xyloglucans (XyGs) are a ubiquitous family of highly branched plant cell wall polysaccharides whose mechanism(s) of degradation in the human gut and consequent importance in nutrition have been unclear. Here we demonstrate that a single, complex gene locus in Bacteroides ovatus confers XyG 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 XyG utilization loci (XyGULs) serve as genetic markers of XyG 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.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4282169/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4282169/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Larsbrink, Johan -- Rogers, Theresa E -- Hemsworth, Glyn R -- McKee, Lauren S -- Tauzin, Alexandra S -- Spadiut, Oliver -- Klinter, Stefan -- Pudlo, Nicholas A -- Urs, Karthik -- Koropatkin, Nicole M -- Creagh, A Louise -- Haynes, Charles A -- Kelly, Amelia G -- Cederholm, Stefan Nilsson -- Davies, Gideon J -- Martens, Eric C -- Brumer, Harry -- BB/I014802/1/Biotechnology and Biological Sciences Research Council/United Kingdom -- DK084214/DK/NIDDK NIH HHS/ -- GM099513/GM/NIGMS NIH HHS/ -- K01 DK084214/DK/NIDDK NIH HHS/ -- R01 GM099513/GM/NIGMS NIH HHS/ -- England -- Nature. 2014 Feb 27;506(7489):498-502. doi: 10.1038/nature12907. Epub 2014 Jan 19.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉1] Division of Glycoscience, School of Biotechnology, Royal Institute of Technology (KTH), AlbaNova University Centre, 106 91 Stockholm, Sweden [2]. ; 1] Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109, USA [2]. ; 1] Structural Biology Laboratory, Department of Chemistry, University of York, York YO10 5DD, UK [2]. ; 1] Division of Glycoscience, School of Biotechnology, Royal Institute of Technology (KTH), AlbaNova University Centre, 106 91 Stockholm, Sweden [2] Wallenberg Wood Science Center, Royal Institute of Technology (KTH), Teknikringen 56-58, 100 44 Stockholm, Sweden. ; Michael Smith Laboratories and Department of Chemistry, University of British Columbia, 2185 East Mall, Vancouver, British Columbia V6T 1Z4, Canada. ; Division of Glycoscience, School of Biotechnology, Royal Institute of Technology (KTH), AlbaNova University Centre, 106 91 Stockholm, Sweden. ; Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109, USA. ; Michael Smith Laboratories and Department of Chemical and Biological Engineering, University of British Columbia, 2185 East Mall, Vancouver, British Columbia V6T 1Z4, Canada. ; Structural Biology Laboratory, Department of Chemistry, University of York, York YO10 5DD, UK. ; 1] Division of Glycoscience, School of Biotechnology, Royal Institute of Technology (KTH), AlbaNova University Centre, 106 91 Stockholm, Sweden [2] Michael Smith Laboratories and Department of Chemistry, University of British Columbia, 2185 East Mall, Vancouver, British Columbia V6T 1Z4, Canada.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/24463512" target="_blank"〉PubMed〈/a〉
Keywords:
Amino Acid Sequence
;
Bacteroides/enzymology/*genetics/growth & development/*metabolism
;
Carbohydrate Metabolism/genetics
;
Carbohydrate Sequence
;
Cell Wall/chemistry
;
Crystallography, X-Ray
;
Diet
;
Dietary Fiber
;
Evolution, Molecular
;
Gastrointestinal Tract/*microbiology
;
Genetic Loci/*genetics
;
Glucans/chemistry/*metabolism
;
Glycoside Hydrolases/chemistry/genetics/metabolism
;
Humans
;
Metagenome
;
Models, Molecular
;
Molecular Sequence Data
;
Phylogeny
;
Protein Structure, Tertiary
;
Symbiosis
;
Xylans/chemistry/*metabolism
Print ISSN:
0028-0836
Electronic ISSN:
1476-4687
Topics:
Biology
,
Chemistry and Pharmacology
,
Medicine
,
Natural Sciences in General
,
Physics
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