The Gut Microbiota: Evidence For Gut Microbes as Contributors to Weight Gain

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1 The Gut Microbiota: Evidence For Gut Microbes as Contributors to Weight Gain Michael T. Bailey, Ph.D. Center for Microbial Pathogenesis The Research Institute, Nationwide Children s Hospital Department of Pediatrics, College of Medicine The Ohio State University Institute for Behavioral Medicine Research, College of Medicine The Ohio State University

2 The Body is Colonized by an Enormous Array of Bacteria Outnumbers Cells of the Body 10:1 Outnumber Human Genes 100:1 Sender et al., Cell, :1

3 The term microbiota refers to the collective microbial community inhabiting a specific environment. Highest Density of Microbes in the Body is Found in the Gut bacteria per gram of contents O Hara and Shanahan, EMBO Rep. 7: (2006) Spor et al., Nature Reviews Microbiology 9: (2011)

4 The majority of the colonic microbiota are in the Firmicutes and the Bacteroidetes phyla Hundreds of bacterial genera and species potentially thousands of bacterial strains Bacterial Phyla Phylogenetic Tree of Life Kingdom Phylum (<10) Class Order Family Predominant Phyla in Gut Firmicutes Ruminococcus spp. Clostridium spp. Lactobacillus spp. Eubacterium spp. Faecalibacterium spp. Roseburia spp. Genus (>200) Species (>500) Bacteroidetes Bacteroides spp. Prevotella spp. [Strain (>10,000)] Spor et al., Nature Reviews Microbiology 9: (2011) Xylanibacter spp.

5 The structure of the intestinal microbiota is associated with the function of the intestinal microbiota. Firmicutes Ruminococcus spp. Clostridium spp. The beneficial Lactobacillus effects spp. that the Eubacterium microbiota spp. have Faecalibacterium on the host is spp. generally Roseburia referred spp. to as their Bacteroidetes function. Bacteroides spp. Prevotella spp. Xylanibacter spp. Relative proportions and abundances of microbes is referred to as the structure of the microbiota. O Hara and Shanahan, EMBO Rep. 7: (2006)

6 How do you study microbial communities? Culture-Based Traditional Microbiology Collect a stool sample Dilute it and grow bacteria on differential/selective agars Gram-negative Bacteria Gram-Positive Bacteria Lactobacillus spp. Bacteria Count colonies and calculate bacterial density

7 How do you study microbial communities? Culture-Based Traditional Microbiology Many anaerobes are strict anaerobes Trace amounts of oxygen is toxic Have to know culture conditions Approximately 80% of intestinal microbes are not easily cultured Thus, can not easily analyze communities, only a few hardy microbes

8 How do you study microbial communities? Sequencing-Based Microbiology 97% Amplicon sequencing metagenomics

9 How do you study microbial communities? Sequencing-Based Microbiology Massive Amounts of Data Identify hundreds to thousands of bacteria per individual Identify all the bacteria in a location (not just 1 or 2 types) Study microbial communities, rather than a single bacterial type

10 Characterization of Microbial Community Diversity Alpha Diversity: Diversity within each sample. Shannon Diversity Index is a measure of both the richness and eveneness of species. Richness: the number of different species present. Eveneness: the abundance of all of the different species. Beta Diversity: Diversity between samples Unifrac distance: places sequences within a phylogenetic tree and compares the trees from sequences in each sample. The distances are put into a matrix and plotted on a principal coordinate plot.

11 Characterization of Microbial Community Calculate relative abundance at any taxonomic level (phylum through genus) Example from: Zhang et al., Nature, 2015

12 Healthy Colonic Microbial Communities Predominance of: Firmicutes Bacteroidetes Majority of microbes Loss of Diversity Is Detrimental: Diversity protects against pathogen infection Loss of diversity opens an ecological niche for pathogens to colonize and potentially overgow (Same ecological principles that are involved in environmental susceptibility to invasive species)

13 Disruptions to structure are associated with diverse diseases. Critically Ill Recipient Donor Patients with antibiotic-associated C. difficile infection - Loss of microbial diversity (often a bloom of proteobacteria). - Prevailing idea is that antibioticinduced loss of diversity is key. Procedure Collect stool sample Extract DNA Amplify bacterial DNA Sequence amplicons Calculate relative abundance of bacterial Phyla. - Most effective treatment is to restore diversity. - How do you restore diversity? Fecal Transplant Shahinas et al., MBio 2012

14

15 Intestinal Infectious Diseases Loss of microbial diversity (fewer microbial types in gut) Overgrowth of pathogen or of microbiota Restoration of diversity (introducing more types of microbes into the gut) is protective Infectious diseases Viral disease Bacterial disease Too Much Diversity has been implicated in inflammatory diseases, such as the inflammatory diseases

16 But, what about obesity? Genetically Obese Mice ob/ob Genetically knockout gene for leptin production Deficiency in satiety hormone (leptin) Overeat (consume 42% more chow) and gain weight Cecal contents were removed Bacterial colonies cloned DNA isolated from clones sequenced Identified 5,088 bacterial sequences (approximately 200/mouse) Calculate the percentage of Bacteroidetes Firmicutes Body Mass (g) Body Mass * Wildtype Ob/Ob Fat Mass (mg) Epididymal fat-pad * Wildtype Ob/Ob Ley et al., Proceedings of the National Academy of Sciences of the USA, 2005

17 What about diet-induced obesity? Mice Fed: 1. CHO Normal Diet Carbohydrate rich, low fat 3.0 Kcal/g 4.5% Fat (by weight) Majority Soybean Oil 40.5% Carbohydrates 2. Westernized Diet High fat, High sugar diet 4.5 Kcal/g 20.3% Fat (by weight) 10% Beef tallow 10% vegatable shortening 19.2% Sucrose (by weight) Bacterial Analysis Cecal contents were removed Bacterial colonies cloned DNA isolated from clones sequenced Identified 7,680 bacterial sequences Calculate the percentage of Bacteroidetes Firmicutes Turnbaugh et al., Cell Host & Microbe, 2008

18 There is an association between obesity and changes in the microbiota, but do the microbiota contribute to weight gain?

19 Do the altered microbiota contribute to weight gain? Use of Germ-Free Mice Breeding Pairs Derived Via C-Section Housed and Bred in Sterile Conditions Advantages 1. Mice Are Completely Sterile 2. Have never come into contact with ANY bacteria, viruses, or fungi Disadvantages 1. Underdeveloped Innate Immunity 2. Altered development of GI tract 3. Developed in unique environment (i.e., bubble isolators)

20 Do the altered microbiota contribute to weight gain? Conventional Mouse Conventionalized Mouse Germ-Free Mouse Contribution of Gut Bacteria to Host Weight Gain Can be Determined by Comparing Germ-Free Mice To Conventional Mice AND Conventionalized Mice

21 Germfree Mice Eat More But Have Lower % Body Fat Backhed et al., Proceedings of the National Academy of Sciences of the USA, 2004 Colonizing germfree mice with microbiota from conventional mice causes them to eat less and gain more weight, suggesting the microbiota are involved in weight gain.

22 If bacteria impact body fat accumulation, and if obese mice have altered microbial populations, does this mean that microbiota are causally involved in the development of overweight/ obesity?

23 Do the altered microbiota contribute to weight gain? Transplant to Germfree Mouse Transplant to Germfree Mouse Turnbaugh et al., Cell Host & Microbe, 2008

24 In rodents, altered profiles of microbiota can lead to weight gain. Obesity is associated with a shift in Bacteroidetes:Firmicutes ratio Genetically obese mice Diet-induced obesity Observed in some, but not all studies The obese microbiota can cause increased weight gain Studies utilizing microbiota transplantation Metagenomic studies demonstrate that obese microbiota are better equipped to extract calories from the diet

25 Rodent biology is a good reflection of human biology, but.. humans and mice are in fact different!

26 Is Microbial Community Structure Altered in the Intestines of Obese Individuals? Longitudinal Study of 12 Obese Individuals Diet: Fat restricted Carbohydrate restricted Stool microbiota sequenced 18,348 sequences Ratio of Firmicutes:Bacteroidetes Obese individuals have higher Firmicutes and lower Bacteroidetes. Losing >6% body mass correlated with a normalization of Firmicutes:Bacteroidetes (regardless of diet/restriction type). Ley et al., Nature, 2006

27 Is Microbial Community Structure Altered in the Intestines of Obese Individuals? Yes! Some (but not all) studies report differences in Firmicutes and Bacteroidetes Remaining Questions: Does it matter? If so, how do changes in the microbiota contribute to weight gain?

28 Commensal microbes from obese twins promote weight gain. Different Microbial Community Structure Principal Coordinate Plot Ridaura et al., Science, 2013

29 Commensal microbes from obese twins promote weight gain. Transplant Microbiota Transplant Microbiota Ridaura et al., Science, 2013

30 Commensal microbes from obese twins promote weight gain. Mice Maintain Human Microbiota Community Structure Ridaura et al., Science, 2013

31 Commensal microbes from obese twins promote weight gain. Transplant Microbiota Transplant Microbiota Ridaura et al., Science, 2013

32 Commensal microbes from obese twins promote weight gain. Microbiota form obese twins lead to more weight gain Ridaura et al., Science, 2013

33 Is Microbial Community Structure Altered in the Intestines of Obese Individuals? Yes! Some (but not all) studies report differences in Firmicutes and Bacteroidetes Remaining Questions: Does it matter? YES!!! If so, how do changes in the microbiota contribute to weight gain?

34 How might intestinal microbes contribute to weight gain? Metabolomics Hundreds of metabolites in the mouse circulation are derived from or modified by the microbiota. (Wikoff et al., 2009) Hartstra et al., 2015 Which metabolites should be studied? The ileum and colon harbors the largest density of microbes Metabolites (or digestive products) that can be absorbed in the ileum or colon.

35 Overweight and obese individuals have higher SCFA levels Short chain fatty acids (SCFA) -butyrate, proprionate, acetate -produced by bacterial fermentation of complex carbohydrates Schwiertz et al., 2013

36 Overweight and obese individuals have higher SCFA levels Short chain fatty acids (SCFA) -butyrate, proprionate, acetate -produced by bacterial fermentation of complex carbohydrates -absorbed through transporters in the gut epithelium (e.g., SLC5A8) -bind to G-protein coupled receptors (e.g., GPR41 and GPR43)

37 Microbial-induced weight gain does not occur in mice lacking the SCFA receptor GPR41 Fat Pad Body Weight Samuel et al., 2008

38 Microbial-produced short chain fatty acids contribute to weight gain SCFA Homeostasis Disruption of SCFA Homeostasis Hartstra et al., 2015

39 How might intestinal microbes contribute to weight gain? Bile acids, cholic acid and chenodexycholic acid, are conjugated to glycine in humans. Conjugated bile acids are taken up in the ileum. Bacteria in the ileum can deconjugate the bile acids so that they can bind to bile acid receptors. Primary bile acids can bind to a nuclear receptor (Farnesoid X Receptor FXR) to regulate lipoprotein and glucose metabolism Are microbiota effects on weight gain dependent upon FXR signaling? Hartstra et al., 2015

40 Microbial-induced weight gain does not occur in mice lacking the farnesoid receptor Microbe-induced weight gain is dependent upon signaling through the Fxr bile acid receptor Parseus et al., 2016

41 Conclusions 1. Overweight and obesity are associated with changes in the composition of the gut microbiota. In mice, genetic obesity and diet-induced obesity Majority of studies find differences in beta diversity Some studies find differences in the ratio of Firmicutes: Bacteroides (this is still controversial). 2. Different microbial communities can contribute to weight gain. Evidence in germfree mice that the microbiota contribute to weight gain Transplanting microbiota from obese humans causes mice to become obese 3. Mechanisms through which microbiota can contribute to weight gain involve microbial production or modification of metabolites. Short chain fatty acids and receptor signaling Modification of bile acids and signaling through the farsenoid receptor

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