Intestinal microbiota in metabolic diseases

The trillions of bacterial cells that colonize the mammalian digestive tract influence both host physiology and the fate of dietary compounds. Gnotobionts and fecal transplantation have been instrumental in revealing the causal role of intestinal bacteria in energy homeostasis and metabolic dysfunctions such as type-2 diabetes. However, the exact contribution of gut bacterial metabolism to host energy balance is still unclear and knowledge about underlying molecular mechanisms is scant. We have previously characterized cecal bacterial community functions and host responses in diet-induced obese mice using omics approaches. Based on these studies, we here discuss issues on the relevance of mouse models, give evidence that the metabolism of cholesterol-derived compounds by gut bacteria is of particular importance in the context of metabolic disorders and that dominant species of the family Coriobacteriaceae are good models to study these functions.

[1]  A. H. Eggerth.  The Gram-positive Non-spore-bearing Anaerobic Bacilli of Human Feces , 1935, Journal of bacteriology.

[2]  V. Bokkenheuser,et al.  Isolation and characterization of human fecal bacteria capable of 21-dehydroxylating corticoids , 1977, Applied and environmental microbiology.

[3]  A. E. Ritchie,et al.  New markers for Eubacterium lentum , 1979, Applied and environmental microbiology.

[4]  A. E. Ritchie,et al.  Isolation and characterization of fecal bacteria capable of 16 alpha-dehydroxylating corticoids , 1980, Applied and environmental microbiology.

[5]  B. Wostmann.  The germfree animal in nutritional studies. , 1981, Annual review of nutrition.

[6]  G. Everson,et al.  Contraceptive steroids alter the steady-state kinetics of bile acids. , 1988, Journal of lipid research.

[7]  S. Kneip,et al.  Direct regulation of bile secretion by prostaglandins in perfused rat liver , 1994, Hepatology.

[8]  Y. Benno,et al.  Rapid Detection of Human Fecal Eubacterium Species and Related Genera by Nested PCR Method , 2001, Microbiology and immunology.

[9]  James R. Cole,et al.  The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy , 2003, Nucleic Acids Res..

[10]  Ting Wang,et al.  The gut microbiota as an environmental factor that regulates fat storage. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Doré,et al.  Intestinal Bacterial Communities That Produce Active Estrogen-Like Compounds Enterodiol and Enterolactone in Humans , 2005, Applied and Environmental Microbiology.

[12]  E. Mardis,et al.  An obesity-associated gut microbiome with increased capacity for energy harvest , 2006, Nature.

[13]  Dae-Joong Kang,et al.  Bile salt biotransformations by human intestinal bacteria Published, JLR Papers in Press, November 18, 2005. , 2006, Journal of Lipid Research.

[14]  L. Jost.  Entropy and diversity , 2006 .

[15]  H. Flint,et al.  Reduced Dietary Intake of Carbohydrates by Obese Subjects Results in Decreased Concentrations of Butyrate and Butyrate-Producing Bacteria in Feces , 2006, Applied and Environmental Microbiology.

[16]  C. Knauf,et al.  Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia , 2007, Diabetologia.

[17]  Masashi Yanagisawa,et al.  Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41 , 2008, Proceedings of the National Academy of Sciences.

[18]  H. Flint,et al.  Human colonic microbiota associated with diet, obesity and weight loss , 2008, International Journal of Obesity.

[19]  J. Doré,et al.  Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients , 2008, Proceedings of the National Academy of Sciences.

[20]  L. Fulton,et al.  Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. , 2008, Cell host & microbe.

[21]  Rob Knight,et al.  High-fat diet determines the composition of the murine gut microbiome independently of obesity. , 2009, Gastroenterology.

[22]  Christophe Caron,et al.  Towards the human intestinal microbiota phylogenetic core. , 2009, Environmental microbiology.

[23]  G. Brinkworth,et al.  Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. , 2009, The British journal of nutrition.

[24]  M. Reilly,et al.  Experimental Endotoxemia Induces Adipose Inflammation and Insulin Resistance in Humans , 2009, Diabetes.

[25]  R. Knight,et al.  The Effect of Diet on the Human Gut Microbiome: A Metagenomic Analysis in Humanized Gnotobiotic Mice , 2009, Science Translational Medicine.

[26]  T. van de Wiele,et al.  Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability , 2009, Gut.

[27]  D. Haller,et al.  Isolation of bacteria from the ileal mucosa of TNFdeltaARE mice and description of Enterorhabdus mucosicola gen. nov., sp. nov. , 2009, International journal of systematic and evolutionary microbiology.

[28]  Yong-hui Shi,et al.  Effects of duodenal redox status on calcium absorption and related genes expression in high-fat diet-fed mice. , 2010, Nutrition.

[29]  R. Ley,et al.  Metabolic Syndrome and Altered Gut Microbiota in Mice Lacking Toll-Like Receptor 5 , 2010, Science.

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

[31]  A. Schwiertz,et al.  Microbiota and SCFA in Lean and Overweight Healthy Subjects , 2010, Obesity.

[32]  M. Blaut,et al.  Absence of intestinal microbiota does not protect mice from diet-induced obesity , 2010, British Journal of Nutrition.

[33]  P. François,et al.  Altered Gut Microbiota and Endocannabinoid System Tone in Obese and Diabetic Leptin-Resistant Mice: Impact on Apelin Regulation in Adipose Tissue , 2011, Front. Microbio..

[34]  E. Want,et al.  Colonization-Induced Host-Gut Microbial Metabolic Interaction , 2011, mBio.

[35]  Jonathan Krakoff,et al.  Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. , 2011, The American journal of clinical nutrition.

[36]  J. Gordon,et al.  Human nutrition, the gut microbiome and the immune system , 2011, Nature.

[37]  S. Heymsfield,et al.  Individual differences in apparent energy digestibility are larger than generally recognized. , 2011, The American journal of clinical nutrition.

[38]  H. Daniel,et al.  C57Bl/6 N mice on a western diet display reduced intestinal and hepatic cholesterol levels despite a plasma hypercholesterolemia , 2012, BMC Genomics.

[39]  Patrice D Cani,et al.  Interaction between obesity and the gut microbiota: relevance in nutrition. , 2011, Annual review of nutrition.

[40]  Yunwei Wang,et al.  Dietary fat-induced taurocholic acid production promotes pathobiont and colitis in IL-10−/− mice , 2012, Nature.

[41]  S. Rabot,et al.  Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice , 2012, Gut.

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

[43]  Yunwei Wang,et al.  Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il 10 2 / 2 mice , 2012 .

[44]  Katherine H. Huang,et al.  A framework for human microbiome research , 2012, Nature.

[45]  Hongzhe Li,et al.  Associating microbiome composition with environmental covariates using generalized UniFrac distances , 2012, Bioinform..

[46]  F. Tinahones,et al.  Endotoxin increase after fat overload is related to postprandial hypertriglyceridemia in morbidly obese patients , 2012, Journal of Lipid Research.

[47]  H. Daniel,et al.  Diet-induced obesity in ad libitum-fed mice: food texture overrides the effect of macronutrient composition , 2012, British Journal of Nutrition.

[48]  W. D. de Vos,et al.  Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women , 2012, Gut.

[49]  E. Zoetendal,et al.  Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. , 2012, Gastroenterology.

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

[51]  C. Mathieu,et al.  Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. , 2012, The Journal of clinical investigation.

[52]  K. Eskridge,et al.  Diet-Induced Alterations of Host Cholesterol Metabolism Are Likely To Affect the Gut Microbiota Composition in Hamsters , 2012, Applied and Environmental Microbiology.

[53]  P. Turnbaugh.  Microbiology: Fat, bile and gut microbes , 2012, Nature.

[54]  J. Stockman,et al.  Metabolic Syndrome and Altered Gut Microbiota in Mice Lacking Toll-Like Receptor 5 , 2012 .

[55]  Lucie Geurts,et al.  Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity , 2013, Proceedings of the National Academy of Sciences.

[56]  M. Hattori,et al.  Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota , 2013, Nature.

[57]  M. Rychlik,et al.  High Fat Diet Accelerates Pathogenesis of Murine Crohn’s Disease-Like Ileitis Independently of Obesity , 2013, PloS one.

[58]  L. Ursell,et al.  Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. , 2013, Gastroenterology.

[59]  Fredrik H. Karlsson,et al.  Gut metagenome in European women with normal, impaired and diabetic glucose control , 2013, Nature.

[60]  W. Wanek,et al.  Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing , 2013, Proceedings of the National Academy of Sciences.

[61]  J. Gordon,et al.  Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut , 2013, Proceedings of the National Academy of Sciences.

[62]  F. Bäckhed,et al.  Microbial modulation of energy availability in the colon regulates intestinal transit. , 2013, Cell host & microbe.

[63]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[64]  I. Martínez,et al.  Gut microbiome composition is linked to whole grain-induced immunological improvements , 2012, The ISME Journal.

[65]  R. Korpela,et al.  A novel mechanism for gut barrier dysfunction by dietary fat: epithelial disruption by hydrophobic bile acids. , 2013, American journal of physiology. Gastrointestinal and liver physiology.

[66]  Na-Ri Shin,et al.  An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice , 2013, Gut.

[67]  H. Daniel,et al.  Properties of myenteric neurones and mucosal functions in the distal colon of diet‐induced obese mice , 2013, The Journal of physiology.

[68]  P. Gérard.  Metabolism of Cholesterol and Bile Acids by the Gut Microbiota , 2013, Pathogens.

[69]  P. Bork,et al.  Richness of human gut microbiome correlates with metabolic markers , 2013, Nature.

[70]  D. Raoult,et al.  Non contiguous-finished genome sequence and description of Enorma massiliensis gen. nov., sp. nov., a new member of the Family Coriobacteriaceae , 2013, Standards in genomic sciences.

[71]  B. Kuster,et al.  High-fat diet alters gut microbiota physiology in mice , 2013, The ISME Journal.

[72]  J. Doré,et al.  Replication of Obesity and Associated Signaling Pathways Through Transfer of Microbiota From Obese-Prone Rats , 2014, Diabetes.

[73]  Alan W Walker,et al.  Phylogeny, culturing, and metagenomics of the human gut microbiota. , 2014, Trends in microbiology.

[74]  P. Lepage,et al.  The Family Coriobacteriaceae , 2014 .

[75]  J. Voorde.  Regulation of vascular tone by adipocytes , 2014 .