The abundance and variety of carbohydrate-active enzymes in the human gut microbiota

Descriptions of the microbial communities that live on and in the human body have progressed at a spectacular rate over the past 5 years, fuelled primarily by highly parallel DNA-sequencing technologies and associated advances in bioinformatics, and by the expectation that understanding how to manipulate the structure and functions of our microbiota will allow us to affect health and prevent or treat diseases. Among the myriad of genes that have been identified in the human gut microbiome, those that encode carbohydrate-active enzymes (CAZymes) are of particular interest, as these enzymes are required to digest most of our complex repertoire of dietary polysaccharides. In this Analysis article, we examine the carbohydrate-digestive capacity of a simplified but representative mini-microbiome in order to highlight the abundance and variety of bacterial CAZymes that are represented in the human gut microbiota.

[1]  Qiang Feng,et al.  A metagenome-wide association study of gut microbiota in type 2 diabetes , 2012, Nature.

[2]  Peter Williams,et al.  IMG: the integrated microbial genomes database and comparative analysis system , 2011, Nucleic Acids Res..

[3]  B. Henrissat,et al.  Structures and mechanisms of glycosyl hydrolases. , 1995, Structure.

[4]  Katherine H. Huang,et al.  Structure, Function and Diversity of the Healthy Human Microbiome , 2012, Nature.

[5]  E. Martens,et al.  How glycan metabolism shapes the human gut microbiota , 2012, Nature Reviews Microbiology.

[6]  G. Michel,et al.  Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota , 2010, Nature.

[7]  J. Gordon,et al.  Functional Genomic and Metabolic Studies of the Adaptations of a Prominent Adult Human Gut Symbiont, Bacteroides thetaiotaomicron, to the Suckling Period* , 2006, Journal of Biological Chemistry.

[8]  Brian J. Bennett,et al.  Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease , 2011, Nature.

[9]  J. Clemente,et al.  Human gut microbiome viewed across age and geography , 2012, Nature.

[10]  H. Flint,et al.  Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon , 2012, The ISME Journal.

[11]  E. Zoetendal,et al.  Victivallis vadensis gen. nov., sp. nov., a sugar-fermenting anaerobe from human faeces. , 2003, International journal of systematic and evolutionary microbiology.

[12]  E. Purdom,et al.  Diversity of the Human Intestinal Microbial Flora , 2005, Science.

[13]  Benjamin P. Westover,et al.  Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont , 2005, Science.

[14]  B. Roe,et al.  A core gut microbiome in obese and lean twins , 2008, Nature.

[15]  G J Davies,et al.  Glycosyltransferases: structures, functions, and mechanisms. , 2008, Annual review of biochemistry.

[16]  Richard A. Flavell,et al.  Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity , 2012, Nature.

[17]  T. Imanaka,et al.  The concept of the α-amylase family: Structural similarity and common catalytic mechanism , 1999 .

[18]  D. Jonkers,et al.  Review article: the role of butyrate on colonic function , 2007, Alimentary pharmacology & therapeutics.

[19]  O. Paliy,et al.  High-Throughput Quantitative Analysis of the Human Intestinal Microbiota with a Phylogenetic Microarray , 2009, Applied and Environmental Microbiology.

[20]  Bernard Henrissat,et al.  Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts , 2011, PLoS biology.

[21]  S. Foster,et al.  Bacterial peptidoglycan (murein) hydrolases. , 2008, FEMS microbiology reviews.

[22]  Bernard Henrissat,et al.  Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. , 2006, Protein engineering, design & selection : PEDS.

[23]  Brandi L. Cantarel,et al.  The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics , 2008, Nucleic Acids Res..

[24]  B Henrissat,et al.  A classification of glycosyl hydrolases based on amino acid sequence similarities. , 1991, The Biochemical journal.

[25]  H. Hamer.  Short chain fatty acids and colonic health , 2009 .

[26]  M. Sakamoto,et al.  Bacteroides plebeius sp. nov. and Bacteroides coprocola sp. nov., isolated from human faeces. , 2005, International journal of systematic and evolutionary microbiology.

[27]  J. Lattimer,et al.  Effects of Dietary Fiber and Its Components on Metabolic Health , 2010, Nutrients.

[28]  J. Slavin,et al.  Low-digestible carbohydrates in practice. , 2008, Journal of the American Dietetic Association.

[29]  A. Bernalier-Donadille.  [Fermentative metabolism by the human gut microbiota]. , 2010, Gastroenterologie clinique et biologique.

[30]  A. Bernalier-Donadille,et al.  Interspecies H2 transfer in cellulose degradation between fibrolytic bacteria and H2-utilizing microorganisms from the human colon. , 2001, FEMS microbiology letters.

[31]  B. White,et al.  Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis , 2008, Nature Reviews Microbiology.

[32]  D. Raoult,et al.  Human Gut Microbiota: Repertoire and Variations , 2012, Front. Cell. Inf. Microbio..

[33]  P. Clifton,et al.  Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. , 2001, Physiological reviews.

[34]  Fredrik H. Karlsson,et al.  Symptomatic atherosclerosis is associated with an altered gut metagenome , 2012, Nature Communications.

[35]  Brandi L. Cantarel,et al.  Complex Carbohydrate Utilization by the Healthy Human Microbiome , 2012, PloS one.

[36]  Bernard Henrissat,et al.  Metabolic Reconstruction for Metagenomic Data and Its Application to the Human Microbiome , 2012, PLoS Comput. Biol..

[37]  P. Bork,et al.  A human gut microbial gene catalogue established by metagenomic sequencing , 2010, Nature.

[38]  B Henrissat,et al.  Structural and sequence-based classification of glycoside hydrolases. , 1997, Current opinion in structural biology.

[39]  H. Flint,et al.  Selective colonization of insoluble substrates by human faecal bacteria. , 2007, Environmental microbiology.

[40]  A. Boraston,et al.  Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes , 2012, Proceedings of the National Academy of Sciences.

[41]  F. Bäckhed,et al.  Obesity alters gut microbial ecology. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A Bairoch,et al.  New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. , 1993, The Biochemical journal.

[43]  P. Čapek,et al.  Dietary fibre degradation and fermentation by two xylanolytic bacteria Bacteroides xylanisolvens XB1AT and Roseburia intestinalis XB6B4 from the human intestine , 2010, Journal of applied microbiology.

[44]  N. Mcneil.  The contribution of the large intestine to energy supplies in man. , 1984, The American journal of clinical nutrition.

[45]  Vincent Lombard,et al.  A hierarchical classification of polysaccharide lyases for glycogenomics. , 2010, The Biochemical journal.

[46]  I-Min A. Chen,et al.  The integrated microbial genomes system: an expanding comparative analysis resource , 2009, Nucleic Acids Res..

[47]  Peer Bork,et al.  Enterotypes of the human gut microbiome , 2011, Nature.

[48]  M. Floch,et al.  Probiotics and functional foods in gastrointestinal disorders , 2002, Current treatment options in gastroenterology.

[49]  A. Macpherson,et al.  Interactions Between the Microbiota and the Immune System , 2012, Science.

[50]  A Bairoch,et al.  Updating the sequence-based classification of glycosyl hydrolases. , 1996, The Biochemical journal.

[51]  B. Henrissat,et al.  Divergence of Catalytic Mechanism within a Glycosidase Family Provides Insight into Evolution of Carbohydrate Metabolism by Human Gut Flora , 2008, Chemistry & biology.