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Downloaded on 2017-02-12T06:38:26Z the Impact of a Variety of Factors on the Obesity Associated Gut Microbiota Title The impact of a variety of factors on the obesity associated gut microbiota Author(s) Clarke, Siobhan F. Publication date 2013 Original citation Clarke, S. F. 2013. The impact of a variety of factors on the obesity associated gut microbiota. PhD Thesis, University College Cork. Type of publication Doctoral thesis Rights © 2013, Siobhan F. Clarke. http://creativecommons.org/licenses/by-nc-nd/3.0/ Item downloaded http://hdl.handle.net/10468/1554 from Downloaded on 2017-02-12T06:38:26Z The impact of a variety of factors on the obesity associated gut microbiota A thesis presented to the National University of Ireland for the degree of Doctor of Philosophy by Siobhan F. Clarke B.Sc. Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland Department of Microbiology, University College Cork, Cork, Ireland Research supervisors: Professor Paul O’Toole and Dr Paul Cotter November 2013 DECLARATION I hereby certify that this material, which I now submit for assessment on the programme of study leading to the award of PhD is entirely my own work, and has not been submitted for another degree, either at University College Cork or elsewhere. Signed:___________________________ Student Number: 105447712 Date:_____________________________ i Table of Content DECLARATION………………………………………………………………………………... i ABSTRACT…………………………………………………………………………………….. ii PUBLICATIONS……………………………………………………………………………….. v ABBREVIATIONS……………………………………………………………………………... INDEX OF TABLES…………………………………………………………………………… INDEX OF FIGURES………………………………………………………………………….. Literary Review: The gut microbiota and its relationship to diet and obesity: new insights 1.1 Abstract……………………………………………………………………………………. 2 1.2 Introduction………………………………………………………………………………... 3 1.3 Gut microbiota of lean and obese animals…………………………………………..... 4 1.3.1 Microbiota of genetically obese mice………………………………………. 4 1.3.2 Microbiota of diet-induced obese mice…………………………………….. 5 1.3.3 Humanized mice ……………………………………………………………… 6 1.4 The composition of the gut microbiota of lean and obese humans…………………. 8 1.4.1 The gut microbiota of lean and obese adult humans……………………... 8 1.4.2 Impact of bariatric surgery on the gut microbiota………………………….. 10 1.4.3 Gut microbiota of normal and overweight pregnant women……………... 11 1.4.4 Gut microbiota of lean and obese children………………………………… 13 1.5 Impact of diet on the gut microbiota……………………………………………………. 15 1.5.1 Low carbohydrate/calorie diets……………………………………………… 15 1.5.2 Other dietary-related influences…………………………………………...... 20 1.6 Manipulation of the gut microbiota……………………………………………………… 23 1.7 Mechanisms by which the gut microbiota may impact on obesity…………………... 29 1.7.1 Energy extraction, Leptin, FIAF and AMPK………………………………... 29 1.7.2 Short chain fatty acids………………………………………………………... 33 1.7.3 LPS-mediated impacts on obesity…………………………………………... 34 1.8 Conclusion………………………………………………………………………………… 38 1.9 References………………………………………………………………………………… 39 CHAPTER II Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity 2.1 Abstract…………………………………………………………………………………….. 56 2.2 Significance of this study…………………………………………………………………. 57 2.3 Introduction………………………………………………………………………………… 58 2.4 Materials and methods……………………………………………………………………. 60 2.4.1 Animals…………………………………………………………………………. 60 2.4.2 Experimental design………………………………………………………...... 60 2.4.3 Probiotic production…………………………………………………………… 60 2.4.4 Weights and tissue sampling…………………………………………………. 61 2.4.5 DNA extractions and amplicon sequencing………………………………… 61 2.4.6 Metabolic markers……………………………………………………………... 61 2.4.7 Statistical analysis…………………………………………………………….. 62 2.5 Results……………………………………………………………………………………… 63 2.5.1 Diet-induced obesity alters the composition of the gut microbiota……….. 63 2.5.2 Vancomycin does not alter the health status of chow-fed mice…………... 64 2.5.3 Vancomycin treatment alters the composition of the gut microbiota in diet-induced obese mice…………………………………………………………….. 64 2.5.4 L salivarius UCC118 alters the composition of the gut microbiota in diet- induced obese mice by a mechanism involving bacteriocin production………... 65 2.5.5 Total bacterial counts were altered by diet-induced obesity and vancomycin treatment, but not by bacteriocin-production by L salivarius UCC118, in diet-induced obese mice………………………………………………. 66 2.5.6 Antimicrobial strategies alter weight gain in diet-induced obese mice....... 66 2.5.7 Vancomycin treatment, but not bacteriocin-production by L salivarius UCC118, improves metabolic markers in diet-induced obese mice……………. 67 2.5.8 Vancomycin treatment is associated with reduced plasma TNFα levels 67 and TNFα mRNA levels in liver and visceral adipose tissues of diet-induced obese mice……………………………………………………………………………. 2.6 Discussion………………………………………………………………………………….. 69 2.7 References…………………………………………………………………………………. 73 2.8 Supporting information……………………………………………………………………. 82 CHAPTER III Targeting the microbiota to address diet-induced obesity: A time dependent challenge 3.1 Abstract…………………………………………………………………………………….. 94 3.2 Introduction………………………………………………………………………………… 95 3.3 Materials and methods……………………………………………………………………. 97 3.3.1 Animals…………………………………………………………………………. 97 3.3.2 Experimental design………………………………………………………....... 97 3.3.3 DNA extraction and high throughput amplicon sequencing………………. 97 3.3.4 Real time quantitative PCR………………………………………………....... 98 3.3.5 Bioinformatic sequence analysis…………………………………………….. 99 3.4 Results……………………………………………………………………………………… 100 3.4.1 α Diversity of the murine gut microbiota increases during the intervention period……………………………………………………………………. 100 3.4.2 Taxonomical analysis highlights the temperal impact of vancomycin on specific components of the gut microbiota………………………………………… 101 3.4.3 UCC118 Bac+ associated reductions in weight gain correspond to reductions in Rikenellaceae and Porphyromonadaceae and increases in Peptococcaceae populations……………………………………………………….. 104 3.4.4 Vancomycin administration reduces total bacterial numbers in the gut…. 106 3.4.5 Beta diversity highlights temporal variation in microbial population…....... 106 3.5 Discussion………………………………………………………………………………….. 108 3.6 References…………………………………………………………………………………. 112 3.7 Supporting information……………………………………………………………………. 122 CHAPTER IV Isogenic strains producing different bile salt hydrolases differ in their impact on weight gain and the composition of the gut microbiota of mice 4.1 Abstract…………………………………………………………………………………….. 131 4.2 Introduction………………………………………………………………………………… 132 4.3 Materials and methods……………………………………………………………………. 134 4.3.1 Bile salt hydrolase cloning and manipulation……………………………….. 134 4.3.2 Animal studies…………………………………………………………………. 134 4.3.2.1 Experimental design - study 1………………………………………. 134 4.3.2.2 Experimental design - study 2………………………………………. 135 4.3.3 DNA extraction and high-throughput DNA sequencing…………………… 135 4.3.4 Analysis of high-throughput DNA sequence data………………………….. 136 4.3.5 Statistical analysis……………………………………………………………... 137 4.4 Results……………………………………………………………………………………… 138 4.4.1 HFD-EC mice gain more weight than controls…………………………....... 138 4.4.2 Caecum microbiota diversity higher in LFD mice relative to HFD controls………………………………………………………………………………… 138 4.4.3 Diet effects microbiota composition in streptomycin treated mice……….. 139 4.4.4 ECBSH1 mice gain less body weight than ECBSH2 mice……………...... 142 4.4.5 Reduced diversity in low fat diet mice in receipt of EC-BSH1……………. 142 4.4.6 Analysis of microbiota beta diversity highlights the dominant impact of BSH1 over diet……………………………………………………………………….. 143 4.4.7 Different sources of BSH impact on specific taxa………………………….. 143 4.4.8 Caecal comparisons reveal that both diet and type of BSH impact on microbiota composition………………………………………………………………. 145 4.4.8.1 BSH activity influences microbiota composition in a strain specific manner……………………………………………………………...... 146 4.5 Discussion………………………………………………………………………………….. 148 4.6 References…………………………………………………………………………………. 153 4.7 Supporting information……………………………………………………………………. 162 CHAPTER V High fat feeding of mice alters their gut microbiota and protects against colitis and colitis-associated colorectal cancer 5.1 Abstract…………………………………………………………………………………….. 194 5.2 Introduction………………………………………………………………………………… 195 5.3 Materials and methods……………………………………………………………………. 198 5.3.1 Animals…………………………………………………………………………. 198 5.3.2 Induction of colitis and colitis-associated colorectal cancer and diet……. 198 5.3.3 Weights and tissue sampling…………………………………………………. 198 5.3.4 Cytokine analysis……………………………………………………………… 199 5.3.5 DNA extraction and 16S rRNA gene amplicon sequencing………………. 199 5.3.6 Bioinformatic analysis of 16s rRNA sequence data……………………….. 200 5.3.7 Statistics………………………………………………………………………… 201 5.4 Results……………………………………………………………………………………… 202 5.4.1 High fat feeding protects mice from inflammation of tumour development 202 5.4.2 High fat diet reduces plasma and colonic cytokines in colitis and CAC model animals………………………………………………………………………… 203 5.4.3 Microbiota diversity is reduced in LF-colitis and LF-CAC mice……...…… 204 5.4.4 Altered gut microbiota composition in animals fed a high fat, rather than a low fat, diet………………………………………………………………………….. 205 5.4.5 The abundance of Proteobacteria in the colitis mouse model is lower in animals fed a high fat diet…………………………………………………………… 206 5.4.6 Proportions of Proteobacteria are also lower in the colitis associated cancer mouse model fed a high fat diet……………………………………………. 207 5.5 Discussion………………………………………………………………………………….
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