Functional Metagenomics and Host Metabolic Interactions in Health and Disease
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1 Merieux, September 8 th 2011 Functional Metagenomics and Host Metabolic Interactions in Health and Disease Jeremy K. Nicholson Head of Department of Surgery and Cancer Faculty of Medicine
2 Supraorganisms Trans-genomic control of metabolism and physiology Multiple interacting gene pools in the body: The Karyome The Chondriome The Microbiome* The Virome* Lederburg, J. (2000) Science Host chromosome set Mitochondrial set Gut, Vaginal, Skin microbial sets Ubiquitous vast gene sets The Epigenome: Karyome-Microbiome Interaction product? *Individuals have unique sets with largely unknown functional capacity. *First microbiome is inherited at birth from mother seeding development of later ecologies
3 A lot of genes and biochemical potential! But what are the microbes actually doing together, how do they interact with the host and how do they vary developmentally, and in physical space and time?
4 Plasmid mediated horizontal pathogen gene transfer to the human microbiome
5 MODELLING GENE-ENVIRONMENT INTERACTIONS IN RELATION TO PERSONAL AND PUBLIC HEALTHCARE Microbiome Exposome Cell (2008) 134:
6 To a systems biologist pathology is just a change in phenotype! Cardiovascular Cancer Metabolic Almost all types of human disease are connected at some genetic level but most common diseases are not genetic in the accepted sense
7 GUT: 2011, /gut
8 GENOME-WIDE ASSOCIATION STUDIES HAVE SIGNIFICANT LIMITATIONS! GIANT study of 249,796 people found 32 statistically significant GWAS BMI linked genes (Nature Genetics, , 2010) Total BMI variance explained = 1.47%! NB: Statistical significance often has little to do with biological significance! 16% of adults with 2 copies of the FTO gene weigh ca. 3kg > adults with 1 FTO copy (& double obesity risk) BUT obesity is about energy balance - diet, exercise, etc.
9 Suggested that Obese Individuals may have a lower Bacteroidetes: Firmicutes ratio than Lean Individuals and this can be modulated by diet.
10 Modern non-infectious human diseases with associated gut microbiotal disorders. Gastric ulcers (Helicobacter pylori) Marshall & Warren (2005 Medicine Nobel Prize) Colonic and other cancers.. Autoimmune (AI) diseases (known) Inflammatory bowel diseases- Ulcerative Colitis & Crohn s (type IV) Type 1 diabetes (type IV)- may be prevented by gut bugs and parasites Primary biliary cirrhosis Celiac disease (type IV hypersensitivity) others too? Insulin resistance related conditions Type 2 diabetes and obesity Allergies & related immune disorders Asthma, Eczema, Psoriasis (suspected AI) Neuropsychiatric disorders Autism, Schizophrenia.(suspected AI) Hypertension.the most important contribution to worldwide mortality?
11 The Primary Metabolome and Co-metabolome interactions (Nicholson, J. et al Nature, Rev. Microbiology, 2005, 3, 2-8) HOST GENOME A B C D E F Cellular transcriptomes Cellular proteomes GUT MICROBIOME Species transcriptomes Species proteomes Species metabolomes Enteron microbial and dietary 2 o metabolites 1 o Intracellular metabolomes Extracellular metabolite pool Co-metabolome enters via hepatic portal + mesenteric veins Biliary secretions enter duodenum from common bile duct Secretory Metabolomes Humans: > 500 functionally distinct NORMAL cell types/ca.10 trillion parenchymal cells ENTEROHEPATIC CIRCULATION Humans: > 1000 Species. > 100 trillion cells
12 Gut Microbes are pharmacologically active and generate or modify signaling molecules: Multiple compound classes from different species and locations - most probably unknown: Short Chain Fatty Acids Bile acids and related oxysterols Vasoactive amines Cresols Endocannabinoids
13 MICROBIAL-MAMMALIAN CO-METABOLISM OF CHOLIC ACID 1. biosynthesis: cholic acid OH COOH HO OH 2. Phase II glycine Conjugation Phase II taurine Conjugation 7. Phase II glycine Conjugation Phase II taurine Conjugation MAMMALIAN LIVER enterohepatic circulation MAMMALIAN GUT HO OH OH C O N H COOH HO OH OH glycocholic acid taurocholic acid 3. secretion into bile amino acid deconjugation by gut microflora 4. regeneration of cholic acid HO OH OH COOH C O N H SO 3H 5. 7-α-dehydroxylation a- by gut microflora H C O N H COOH HO glycodeoxyocholic acid 6. reabsorption into blood via hepatic portal system deoxycholic acid HO H HO H C O N H SO3H taurodeoxyocholic acid 8. secretion into bile 9. Deconjugation further reactions COOH Imperial College, 2007
14 MICROBIOME-MAMMALIAN INTERACTIONS AND CALORIFIC AVAILABILITY * * * Martin, F. et al Mol Syst Biol (2007)
15 PNAS (2011)
16 Gut Microbial Effects on Bile Acid Conjugate Patterns in Multiple Compartments Normal Rats (Taurine Conjugation Dominance in Germ Free) Germ Free Rats UPLC-QToF-MS Quantified Bile Acids Swann, J et al PNAS in press (2010)
17 (2011) Gene Expression Blue: Up regulated in Germ-Free. Red: Down regulated in Germ-Free Hepatic transcriptomic patterns show cholesterol, bile acid synthesis and steroid metabolism are closely linked to gut microbial activities
18 Understanding the role of the microbiome in complex systems events The health enigma of bariatric surgery
19 Bariatric and Metabolic Surgery Roux-en-Y Gastric Bypass Surgery - Gold Standard Sleeve gastrectomy with duodenal switch Vertical banded gastroplasty Adjustable gastric band All give ca kg weight loss over 36 months - can give > 50% loss of XS weight in 12 months. 80% of T2 diabetics cured by Rouxen Y in 24h - mechanism unknown! Significant reduction in colo-rectal and other cancer rates in bariatric patients - mechanism unknown! Roux-en-Y Gastric Bypass
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21 PNAS February 17, 2009 vol. 106 (7) Normal Obese
22 (GUT, May 2011) Experimental Bariatric Surgery in Wistar Rats with Combined Metabonomic and Metagenomic Profiling n = 12 RYGB procedure; n = 12 Sham-Operated Microbiome (454 Pyrosequencing; n= 6 x2), Urine and Fecal Water Analysis 2,4,6, 8 weeks post-operatively
23 Microbiological consequences of the Roux-en-Y bariatric procedure in the Rat (454 pyrosequencing/ PCR amplification of V1-V3/MOTHUR analysis) A Sham 100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Rat 1 Rat 2 Rat 3 Rat 4 Rat 5 Rat 6 w2 w8 w2 w8 w2 w8 w2 w8 w2 w8 w2 w8 Firmicutes p (sham vs. RYGB) w2 w *** RYGB 100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% Rat 7 Rat 8 Rat 9 Rat 10 Rat 11 Rat 12 w2 w8 w2 w8 w2 w8 w2 w8 w2 w8 w2 w8 Bacteroidetes Proteobacteria Actinobacteria * <0.0001*** B week 2 week 8 p (sham vs. RYGB) Sham Actinobacteria w w Bacilli Bacteroidetes * Clostridia 0.012** *** Erysipelotrichi RYGB Gammaproteobacteria Others 0.036* _ <0.0001*** _
24 SHAM NMR-Urinary Metabolite Profiles 8 weeks after the Surgical Procedures RYGB
25 RYGB induces massive changes in fecal bile acid profiles - in particular a reduction in total unconjugated and taurineconjugated bile acids Unconjugated Taurine Conjugated Key: Sham/RYGB
26 Phylogenetic relationships in RYGB/sham operated rats GAKP9UA03F8FRPS06 Gammaproteobacteria 1 GAKP9UA03FU57NB1 1 Betaproteobacteria Legend: Treatment group RYGB SHAM GAKP9UA03F3DRVB05 Gammaproteobacteria 1 GAKP9UA03GYTSWS06 Gammaproteobacteria 1 GAKP9UA03GFQI9S06 Gammaproteobacteria 1 GAKP9UA03HH8X3S06 Gammaproteobacteria 1 GAKP9UA03HD1XQB07 Gammaproteobacteria 1 GAKP9UA03FNKVSB08 Gammaproteobacteria 1 GAKP9UA03GGDEDB08 Gammaproteobacteria 1 GAKP9UA03G9WZOS06 Gammaproteobacteria 1 GAKP9UA03GLPRBB04 Gammaproteobacteria 1 GAKP9UA03FR0AZB07 Gammaproteobacteria 1 GAKP9UA03GD24WB10 Gammaproteobacteria 1 GAKP9UA03GIKIRB05 Gammaproteobacteria 1 GAKP9UA03GU7OMB10 Gammaproteobacteria 1 GAKP9UA03F8872B04 Gammaproteobacteria 1 GAKP9UA03FXNIJB04 Gammaproteobacteria GAKP9UA03GVPI7B09 Gammaproteobacteria 1 Taxonomy: Clostridia Proteobacteria Bacteroidetes GAKP9UA03F9ZQ1S1 1 Clostridiales GAKP9UA03FSX2DB04 Clostridiales GAKP9UA03GDHMZS1 1 Clostridiales GAKP9UA03GWEZLS01 Clostridiales GAKP9UA03F80K8S04 Clostridia GAKP9UA03GZ4ZYB02 Clostridiales GAKP9UA03G9JSNB08 Clostridiales GAKP9UA03G6VZIS07 Clostridiales GAKP9UA03GUH0GS01 Clostridiales GAKP9UA03GGUUCB09 Clostridia GAKP9UA03F6T2AS07 Clostridiales GAKP9UA03F84BQS02 Clostridiales GAKP9UA03GO9OOS05 Clostridiales GAKP9UA03FMNJVS05 Clostridiales GAKP9UA03GVQGXS08 Clostridiales GAKP9UA03FYO81S02 Clostridiales GAKP9UA03G8ZR0S03 Clostridiales GAKP9UA03FZY1GS02 Clostridiales GAKP9UA03FRHGUS05 Clostridiales GAKP9UA03GKFM4S08 Clostridiales GAKP9UA03G9PHXS05 Clostridiales GAKP9UA03G8OB0B01 Clostridiales GAKP9UA03GBN5CS09 Clostridiales GAKP9UA03GZAH9S01 Clostridiales Numbers of 454 reads GAKP9UA03GGB2BS1 1 Clostridiales GAKP9UA03GS7DKS05 Clostridiales GAKP9UA03FL2QLS08 Clostridiales GAKP9UA03GIFUXS08 Clostridiales GAKP9UA03GC6NQS01 Clostridiales GAKP9UA03GKDC0S08 Clostridiales GAKP9UA03GTIS0S09 Clostridiales GAKP9UA03FYZBRS09 Clostridiales GAKP9UA03FTSPXS08 Clostridiales GAKP9UA03F99NXS08 Clostridiales GAKP9UA03GQ8FNS1 1 Clostridiales GAKP9UA03GQ9I3S05 Clostridiales GAKP9UA03GOM51S05 Clostridiales GAKP9UA03FZNC0S08 Clostridiales GAKP9UA03G2JOES01 Clostridiales GAKP9UA03GF4BGS02 Clostridiales GAKP9UA03FXMW1S03 Clostridiales GAKP9UA03G10G1S02 Clostridiales GAKP9UA03GIC96S03 Clostridiales GAKP9UA03HB52MS03 Bacillales Mollicutes GAKP9UA03FOJ6KS06 CMN et rel. GAKP9UA03HB7D4S06 CMN et rel. GAKP9UA03GEJEEB01Actinomycetaceae-Bifidobacteriaceae GAKP9UA03FHVJPS10Actinomycetaceae-Bifidobacteriaceae GAKP9UA03FKKW0B04Actinomycetaceae-Bifidobacteriaceae GAKP9UA03GEABUB12 Bacillales Mollicutes GAKP9UA03FV28WB12 Bacillales Mollicutes GAKP9UA03GTFF3S04 Bacillales Mollicutes GAKP9UA03G19YYB05 Bacillales Mollicutes GAKP9UA03GR60WB03 Bacillales Mollicutes GAKP9UA03FRQG8B03 Bacillales Mollicutes GAKP9UA03GEPE8B02 Bacillales Mollicutes GAKP9UA03FZU02B04 Clostridiales GAKP9UA03GAEWKB01 Clostridiales GAKP9UA03FOY31B12 Clostridiales GAKP9UA03GHY2QB04 Clostridiales GAKP9UA03F7Q9LS04 Bacteroidetes GAKP9UA03GW9V0S05 Bacteroidetes GAKP9UA03FOVCES04 Bacteroidetes GAKP9UA03HCLC6B09 Bacteroidetes GAKP9UA03GJTCBS1 1 Bacteroidetes GAKP9UA03G1ZCKS12 Bacteroidetes GAKP9UA03FZ72FB01 Bacteroidetes GAKP9UA03FYW48B07 Bacteroidetes GAKP9UA03GYC7KS02 Bacteroidetes GAKP9UA03FS94GB01 Bacteroidetes GAKP9UA03HD6UIB10 Bacteroidetes GAKP9UA03FOJHHB10 Bacteroidetes GAKP9UA03GYDIQB10 Bacteroidetes GAKP9UA03GAI96B05 Bacteroidetes GAKP9UA03GX3IBS09 Bacteroidetes GAKP9UA03HERBWB10 Bacteroidetes GAKP9UA03GS2ORS02 Bacteroidetes GAKP9UA03HAR3OB02 Bacteroidetes GAKP9UA03FJ3MGB03 Bacteroidetes GAKP9UA03FYX5RB02 Bacteroidetes GAKP9UA03FUFS7S08 Bacteroidetes GAKP9UA03F81S1S10 Bacteroidetes GAKP9UA03GXJA1S10 Bacteroidetes GAKP9UA03FNH8RS10 Bacteroidetes GAKP9UA03GPHK3S10 Bacteroidetes GAKP9UA03G79A2S10 Bacteroidetes GAKP9UA03GPQDAS10 Bacteroidetes GAKP9UA03FWIGES10 Bacteroidetes GAKP9UA03GOB4QS12 Bacteroidetes GAKP9UA03GFXRUS03 Bacteroidetes GAKP9UA03G1I8TS07 Bacteroidetes GAKP9UA03GJSZGS02 Bacteroidetes GAKP9UA03G0PEYS07 Bacteroidetes GAKP9UA03GJPA3B05 Bacteroidetes GAKP9UA03FPG52S03 Bacteroidetes GAKP9UA03FMCZUS02 Bacteroidetes GAKP9UA03HI8ZCS03 Bacteroidetes GAKP9UA03HA949S01 Bacteroidetes GAKP9UA03GQSFGB08 Bacteroidetes GAKP9UA03FKFGBB08 Bacteroidetes GAKP9UA03HHEVGS08 Bacteroidetes GAKP9UA03GQBB6B02 Bacteroidetes GAKP9UA03GYNHCS04 Bacteroidetes GAKP9UA03GMYA6S01 Bacteroidetes GAKP9UA03G96MSS1 1 Bacteroidetes GAKP9UA03HB45MS01 Bacteroidetes GAKP9UA03FR05ZB02 Bacteroidetes GAKP9UA03GDHAXB1 1 Bacteroidetes GAKP9UA03FKA9BB1 1 Bacteroidetes GAKP9UA03FQTFTB1 1 Bacteroidetes GAKP9UA03HGWQPB1 1 Bacteroidetes * Relative abundance counts 0
27 Specific Microbiome-Metabolome Correlation Projection to an important discriminatory species Enterobacter hormaechi PAG Cre 0.7 Feces Ura Ura PT MA PT Urine IS IS HA PG PG Cre PAG HA PG PS RYGB Sham Correlation Coefficients (a.u.) Asp ppm 0 Transgenomic statistical spectroscopic projections via O2-PLS (microbial-metabolic linkage) to reveal major microbial-metabolic connections in 2 compartments
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29 Supersystem Interactions in Obesity and Cancer Holmes, E. et al Trends in Microbiology (2011) in press
30 Molecular Epidemiology Metabolic Phenotyping Whole Populations in Relation to Disease Risk Factors
31 METABOLOME-WIDE ASSOCIATION STUDY ON LINKAGE OF GUT MICROBIAL METABOLISM WITH HIGH BLOOD PRESSURE AND OBESITY
32 Holmes, E. et al (2008) THE METABOLOME-WIDE ASSOCIATION STUDY (MWAS) CONCEPT The broad non-selective analysis and statistical interrogation of metabolic phenotypes in relation to epidemiologic end-points and risk factors to generate testable physiological or pathway hypotheses.
33 Geographical Metabolic Mapping and Human Disease (INTERMAP) China, Japan, USA, UK - 17 sub-populations, male/female, n = 4800 people sampled x 2 Holmes, E. et al (2008), Nature Mortality,BMI, cardiovascular risk, type 2 diabetes USA UK USA Japan China
34 Principal Population Metabotype Biomarkers (P < 10-6 ) =
35
36 Metabolome-Wide Association Studies: Metabolic biomarkers of high blood pressure and body mass index in Eastern and Western populations Holmes, E. et al (2008), Nature
37 METABOLOME WIDE ASSOCIATION STUDIES: METABOLIC PHENOTYPE LINKAGE TO HUMAN BLOOD PRESURE Holmes, E. et al (2008) Diversity in Human Metabolic Phenotypes and Association with Diet and Blood Pressure. Nature, ,
38 Metabolome-Wide Association Studies for novel hypothesis generation: e.g. Does formate have a role in human BP regulation and can this be modulated via microbiome engineering? Salt intake correlates with high blood pressure CFEX CFEX anion exchanger under inhibitory control of the serine-threonine kinase WNK Hyperoxaluric patients (low gut Oxalobacter sp.) - are markedly hypertensive!
39 THE WAY OF THE FUTURE? Collectively the human microbiome may have > 20 x drugable targets than the human genome! The Age of The Microbiome Pharmacopoeia has Arrived!
40
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