6/24/2014. How do you study microbial communities? Outnumbers Cells of the Body 10:1 Outnumber Human Genes 100:1. Michael T. Bailey, Ph.D.

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1 Interactions between Diet and the Intestinal Microbiota: Implications for Obesity The Body is Colonized by an Enormous Array of Bacteria Outnumbers Cells of the Body 10:1 Outnumber Human Genes 100:1 Michael T. Bailey, Ph.D. Institute for Behavioral Medicine Research, College of Medicine and the Biosciences Division, College of Dentistry The Ohio State University The term microbiota refers to the collective microbial community inhabiting a specific environment. The majority of the colonic microbiota are in the Firmicutes and the Bacteroidetes phyla Highest Density of Microbes in the Body is Found in the Gut bacteria per gram of contents Hundreds of bacterial genera and species potentially thousands of bacterial strains 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. Spor et al., Nature Reviews Microbiology 9: (2011) O Hara and Shanahan, EMBO Rep. 7: (2006) Spor et al., Nature Reviews Microbiology 9: (2011) Genus (>200) Species (>500) [Strain (>10,000)] Bacteroidetes Bacteroides spp. Prevotella spp. Xylanibacter spp. 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 i spp. generally Roseburia referred spp. to as their function. Bacteroidetes 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) 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 1

2 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 can not be cultured Thus, can not analyze communities, only a few hardy microbes How do you study microbial communities? Sequencing-Based Microbiology Collect stool sample Extract DNA Amplify bacterial DNA encoding for rrna using PCR Sequence the amplified bacterial DNA Match sequence to databases containing whole microbial genomes to identify bacteria Classify the bacteria taxonomically (e.g., what Phylum, Class, Order, Family, Genus, Species) Calculate relative abundance of each bacterial type Percentage of total sequences that fall into a specific bacterial type 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 Healthy Colonic Microbial Communities Predominance of: Firmicutes Bacteroidetes Approximately 90-95% A lot of microbial diversity: 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) 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 t antibioticinduced loss of diversity is key. Procedure Collect stool sample Extract DNA Amplify bacterial DNA Sequence amplicons Calculate relative abundance of bacterial Phyla. - Only effective treatment is to restore diversity. - How do you restore diversity? Fecal Transplant Shahinas et al., MBio

3 Intestinal Infectious/Inflammatory Diseases But, what about obesity? 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 Inflammatory diseases Inflammatory bowel diseases 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 DNA isolated and inserted into bacteria for cloning Cloned DNA was sequenced Identified 5,088 bacterial sequences (approximately 200/mouse) Calculate the percentage of Bacteroidetes Firmicutes s (g) Body Mass 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 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 DNA isolated and cloned Clones were sequenced Identified 7,680 bacterial sequences Calculate the percentage of Bacteroidetes Firmicutes There is an association between obesity and changes in the microbiota, but do the microbiota contribute to weight gain? Turnbaugh et al., Cell Host & Microbe, 2008 Do the altered microbiota contribute to weight gain? 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 Conventional Mouse Conventionalized Mouse Advantages 1. Mice Are Completely l 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) 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 3

4 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. Studies with Germfree Mice (i.e., No Bacteria) Support a Link Between Bacteria and Weight Gain Germfree Mice Higher food consumption Lower leptin levels Yet, Lower body mass Lower triglycerides Lower metabolic rate All of this suggests the microbiota are involved with weight gain. Feeding the sterile mice bacteria normalizes weight!!! (Mechanisms by which this occurs are matter of intense study.) 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? Do the altered microbiota contribute to weight gain? Transplant to Germfree Mouse Transplant to Germfree Mouse Turnbaugh et al., Cell Host & Microbe, 2008 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 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 Rodent biology is a good reflection of human biology, but.. humans and mice are in fact different! 4

5 Is Microbial Community Structure Altered in the Intestines of Obese Individuals? 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 30 Obese Individuals (27 Males, 3 Females) Stool samples collected prior to, as well as 3 and 6 mo post-gastric bypass surgery Microbial populations assessed using real-time RT-PCR. Absolute abundance of Bacteroides group of microbes 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 Furet et al., Diabetes, 2010 Obese Post-Gastric Bypass Can the human microbiota contribute to weight gain? Gut microbiota from twins discordant for obesity have different effects on weight gain Gut microbiota from twins discordant for obesity have different effects on weight gain Is Microbial Community Structure Altered in the Intestines of Obese Individuals? Yes! Many (but not all) studies report differences in Firmicutes and Bacteroidetes t Question now, is why???? 29 5

6 What shapes microbial communities? One thought is that there are 3 enterotypes High Bacteroides High Prevotella High Ruminococcus What leads to the development of the enterotype Genetics Functioning of immunity (e.g., Toll-like receptor expression linked to microbiota) Functioning of gastrointestinal physiology (e.g., bile acid composition linked to microbiota) Diet? Are enterotypes related to diet? 29 Healthy Volunteers Diet information Recent diet Queried using food Recall questionnaires Habitual diet Queried using Food Frequency Questionnaires Stool samples collected DNA isolated and amplified 16s rdna gene segments sequenced using 454 pyrosequencing Relative abundance of microbial types determined Correlated the abundance of microbial populations to dietary components from FFQ Bacteroides and Prevotella Enterotype in Healthy Adults Enterotype Correlates with Diet Composition Bacterial Genus Levels Relative abundance of 36 microbes correlated to calculated amount of nutrients in diet based on FFQ responses. Red = positive correlation Blue = negative correlation Diet Compositional Analysis from Food Frequency Quesionnaires n=14 Bacteroides n=15 Prevotella Wu et al., Science 2011 Wu et al., Science 2011 Enterotype Correlates with Diet Composition Enterotype Correlates with Diet Composition Bacteroides Prevotella Bacteroides Prevotella High Bacteroides Correlates with Multiple Amino Acids (and Fats) High Prevotella Correlates With High Sucrose Wu et al., Science 2011 Wu et al., Science

7 Enterotype Correlates with Diet Composition Bacteroides correlates with protein/fats Prevotella with carbohydrates Associations with long-term dietary habits Correlations only significant with FFQ No associations with Food Recall Switching diet did not change the enterotype Transient changes occurred within 24 hrs Enterotype still evident after 10 days of changing diet What shapes colonic microbial communities? Thought that there are 3 enterotypes High Bacteroides High Prevotella High Ruminococcus What leads to the development of the enterotype Genetics Functioning of immunity (e.g., Toll-like receptor expression linked to microbiota) Functioning of gastrointestinal physiology (e.g., bile acid composition linked to microbiota) Diet Carbohydrates Prevotella Protein/Fats Bacteroides Mom? Maternal Microbiota and Infant Colonization Babies are sterile during development in utero and become colonized during birth Early microbes largely derived from the mother Initial microbial communities influence the assemblage of adult-like microbial community By 2 yrs of age, adult-like profile is reached Development of the Baby Belly Study If obesity is associated with an altered profile of microbiota If infant microbiota is inherited from the mother Hypothesis: At 2 years of age, when children have an adult-like microbial profile, children from obese mothers will have different gut microbial communities than children from normal-weight mothers. Spor et al., Nature Reviews Microbiology 2011 Maternal BMI is associated with infant bacterial changes at 1 and 6 months of age Maternal BMI is associated with infant bacterial changes at 1 and 6 months of age But, do these differences persist into the adult-like profile?

8 Baby Belly Study Recruited mothers with infants at 24 (±2) months of age Obese mothers pre-pregnancy BMI 30 Normal weight mothers pre-pregnancy BMI < 30 Questionnaires pertaining to: Pregnancy weight (and weight gain) Pregnancy health behaviors Infant/childhood weight Infant/childhood health behaviors Infant/childhood diet Infant/childhood temperament Collected a stool sample from the diaper Baby Belly Study (continued) Extract DNA Amplified DNAencoding for the V1-V3 region of bacterial 16S rrna Amplicons sequenced using Next-Gen 454 FLX Titanium Pyrosequencing 794,822 sequences for each baby we collected approximately 10,000 Sequences were matched to databases containing known bacterial genomes to identify bacteria Calculate the relative abundance of each bacterial type Relative Abundance = # Identified Sequences # Sequences Colleted X 100 Baby Belly Study 77 Children Aged Months Children from Obese Mothers n = females; 12 males 14 daycare; 12 homecare 22 breastfed; 4 bottlefed 21 white; 5 black 12 C-section; 14 vaginally 3 smokers Children from Non-Obese Mothers n = females; 29 males 19 daycare; 30 homecare 50 breastfed; 1 bottlefed 46 white; 2 black; 3 Asian 21 C-section; 30 vaginally 1 smokers Maternal Obesity is Associated with Higher Alpha Diversity in 2 Year Olds Diversity Index Shannon * Obese Mothers Non-Obese Mothers Interpretation: Overall, there are more types of bacteria in the intestines of kids born to obese mothers. ariance Explained Maternal Obesity is Associated with Differences in Beta Diversity (Unweighted Unifrac Distance Metric) 0.3 Non-Obese Obese Classification of people as lean or obese can be made solely on the basis of their gut microbiota with 90% 0.0 accuracy, but they do not separate into distinct t microbiota-based b -0.1 clusters on commonly used principal coordinate plots, which are used to -0.2 identify statistical differences between groups Non-Obese Mothers Lozupone et al, Nature 2012 Obese Mothers PC1-4.69% of Variance Explained Interpretation: Children from obese mothers have different types of bacteria in their intestines than children from normal-weight mothers. PC2-3.76% of Va otal Sequences Proportion of T Phylum Level Analysis of Microbiota in 2 yr old Children from Obese and Normal Weight Mothers Normal Weight Relative Abundance of Major Phyla Obese Total Sequences Proportion of T Normal Weight Relative Abundance of Major Phyla Obese Interpretation: There is an expansion of Proteobacteria, but ratio of Firmicutes and Bacteroidetes was unaffected by maternal obesity. Firmicutes Bacteroidetes Proteobacteria Other Bacteria Verrucomicrobia Actinobacteria Cyanobacteria Deferribacteres Unclassified 8

9 The relative abundance of important bacterial genera is different in children from obese mothers. The relative abundance of important bacterial genera is different in children from obese mothers. Association of Roseburia Prevalence with BMI Association of Roseburia spp. with BMI Oscillibacter spp. Abundance Faecalibacterium spp. Abundance 30 Relative Abundance of Oscillibacter Obese Mothers Relative Abundance of Faecalibacterium * * Non-Obese Mothers Obese Mothers Non-Obese Mothers % of Total Seq quences Oscillibacter spp. Faecalibacterium spp. Roseburia spp. All members of the Firmicutes All know producers of short chain fatty acids. Maternal BMI Why are producers of short-chain fatty acids important? It is thought that the microbiota contribute approximately kcal/day. (McNeil et al., 1984; Cummings et al., 1997) Approximately 75% of these calories are short- chain fatty acid dependent. (McNeil et al., 1984) Why are producers of short-chain fatty acids important? Bacterial fermentation of oligosaccharides results in production of SCFA. The 3 most predominant are butyrate, acetate, and proprionate. Proprionate and acetate reach peripheral organs and the liver where they are substrates for lipogenesis and gluconeogenesis. Butyrate is absorbed and used by colonic epithelial cells. Can increase receptor expression and affect gene expression by inhibiting histone deacetylase (HDAC). Interpretation: It is possible that the increase in producers of short-chain fatty acids contributes to weight gain over the life of the host. Summary Baby Belly Study Overall changes in both alpha diversity and beta diversity (although no difference in the bacteroidetes and firmicutes) Higher abundance of butyrate producing microbes (which has been associated with weight gain) Does this provide insight into observations that maternal obesity is associated with: Associated with increased weight in infants (American Adacemy of Pediatrics (AAP), Committee on Nutrition, Pediatrics 112: (2003)) Children are twice as likely as developing obesity in preschool years (Whitaker et al., Pediatrics 114: e29-e36 (2004)) Conclusions Weight gain/obesity is associated with altered profiles of intestinal microbiota Evidence in laboratory animals that the microbiota contribute to weight gain Weight loss methods tend to normalize profiles Microbial profiles (or enterotypes) associated with diet Long-term dietary habits predictive of enterotype Protein/Fat-Rich diet associated with Bacteroides Carbohydrate-Rich diet associated Prevotella Altered profiles of microbiota may be passed from mother to infant Contribution to childhood obesity? 9

10 Acknowledgements Bailey Lab Dr. Amy Mackos Jeffrey Galley Mari Couasnon Sydney Fisher Dr. Andrew Tarr Dr. Maria Khan Krysten Clark Ohio State University Dr. Lisa Christian Kelly Marceau Dr. Purnima Kumar Dr. Zhongtang Yu Dr. Diane Habash Dr. Sarah Schoppe- Sullivan Dr. Ihuoma Eneli Research and Testing Laboratory Dr. Scot E. Dowd Funding: National Institutes of Health RO3AI R21AI RO1AT Ohio State University College of Medicine Start Up College of Dentistry Start Up Food Innovation Center Innovative Initiative Pelotonia undergraduate fellowship Mead Johnson Pediatric Nutrition VSL Pharmaceuticals 10

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