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The Metabolism of Plant Glucosinolates by Gut Bacteria

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The Metabolism of Plant Glucosinolates by Gut Bacteria The metabolism of plant glucosinolates by gut bacteria Fatma Cebeci A thesis submitted for the degree of Doctor of Philosophy to the University of East Anglia Institute of Food Research April, 2017 © This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. PhD Thesis 2017 Fatma Cebeci Metabolism of Plant Glucosinolates by Gut Bacteria ABSTRACT Glucosinolates found in cruciferous vegetables are degraded by plant myrosinases into bioactive isothiocyanates (ITCs) which have been recognised as potent anticancer compounds. During cooking, plant myrosinases are heat inactivated so ITC production is dependent on the myrosinase-like enzymes produced by the gut bacteria. This study is focused on investigating glucosinolate metabolism by the human gut bacteria and identifying the enzymes that play a crucial role. Human gut bacteria that were previously reported to metabolise glucosinolates were investigated in this study. In addition, 98 more human gut strains were isolated using a glucoraphanin enrichment method. It was hypothesised that bacterial myrosinases are β- glucosidases with specificity for glucosinolates. To identify the first bacterial myrosinase from the human gut, four putative β-glucosidases from Enterococcus casseliflavus CP1 and Escherichia coli FI10944 were cloned and heterologously expressed in E. coli. An alternative approach using a combination of ion exchange chromatography and gel filtration was also carried out to identify the bacterial myrosinase of E. coli FI109444. It has been reported that some gut bacteria require a reduction step to metabolise methylsulfinylalkyl glucosinolates (such as glucoraphanin) that converts them into methylthioalkyl glucosinolates (such as glucoerucin) to produce ITCs. To identify the responsible reductase, candidate reductase genes were cloned and expressed in E. coli. Methionine sulfoxide reductase B (MsrB) from Escherichia coli VL8 and Lactobacillus agilis R16 was found to reduce glucoraphanin to glucoerucin under the conditions tested. A bacterial myrosinase of Citrobacter WYE1 of soil origin was previously identified and myrosinase activity of this enzyme was characterised using cell-free extracts. In this study the myrosinase gene was heterologously expressed in E. coli to allow purification and characterisation. The recombinant enzyme showed activity against several glucosinolate substrates and protein was produced for crystallographic studies. ii TABLE OF CONTENTS ABSTRACT ....................................................................................................................... ii TABLE OF CONTENTS ...................................................................................................... iii LIST OF FIGURES ........................................................................................................... viii LIST OF TABLES ............................................................................................................. xii OUTPUTS FROM THIS PROJECT ..................................................................................... xiv ABBREVIATIONS............................................................................................................ xv ACKNOWLEDGEMENTS .............................................................................................. xviii 1 GENERAL INTRODUCTION ............................................................................................ 1 1.1 GLUCOSINOLATES ................................................................................................ 2 1.1.1 General Structure and Biological Importance of Glucosinolates ......................... 2 1.1.2 Glucosinolate Biosynthesis ................................................................................... 7 1.2 GLUCOSINOLATE HYDROLYSIS AND DEGRADATION PRODUCTS ........................... 11 1.2.1 ITC Formation ..................................................................................................... 13 1.2.2 Nitrile and Epithionitrile Formation.................................................................... 14 1.2.3 Thiocyanate Formation ....................................................................................... 14 1.2.4 Other Products.................................................................................................... 15 1.3 THE IMPORTANCE OF GLUCOSINOLATES AND THEIR DEGRADATION PRODUCTS .. 15 1.3.1 Chemopreventative effects of Glucosinolates and ITCs ..................................... 15 1.3.2 Protective Effects of Glucosinolates and ITCs against Diseases ......................... 17 1.3.3 Toxicity of Glucosinolates and Their Degradation Products .............................. 18 1.4 BIOAVAILABILITY OF GLUCOSINOLATES AND THEIR DEGRADATION PRODUCTS ... 19 1.5 MYROSINASES .................................................................................................... 23 1.6 METHIONINE SULPHOXIDE REDUCTASES ............................................................. 27 1.7 GUT MICROBIOTA .............................................................................................. 30 1.8 THE ROLE OF GUT MICROBIOTA IN BIOTRANSFORMATION OF DIETARY COMPOUNDS ................................................................................................................ 36 iii 1.9 GLUCOSINOLATE METABOLISM BY GUT BACTERIA .............................................. 37 1.10 SCOPE OF THE THESIS ......................................................................................... 41 2 GENERAL MATERIALS AND METHODS ........................................................................ 43 2.1 MICROBIOLOGY METHODS ................................................................................. 44 2.1.1 Culture Media ..................................................................................................... 44 2.1.2 Preparation of Antibiotic Stock Solutions ........................................................... 45 2.1.3 Isolation of Glucosinolate Degrading Bacteria by Glucoraphanin Enrichment .. 45 2.1.4 Bacterial Strains and Culture Conditions ............................................................ 46 2.1.5 Bacterial Growth Analysis ................................................................................... 46 2.1.6 Scanning Electron Microscopy (SEM) ................................................................. 47 2.2 MOLECULAR BIOLOGY ........................................................................................ 47 2.2.1 Polymerase Chain Reaction (PCR) ...................................................................... 47 2.2.2 Gel Electrophoresis ............................................................................................. 48 2.2.3 Plasmid Preparation ........................................................................................... 48 2.2.4 Enzyme Restrictions ............................................................................................ 49 2.2.5 Dephosphorylation of Digested Plasmids ........................................................... 49 2.2.6 Primer Design ..................................................................................................... 49 2.2.7 PCR Product Purification ..................................................................................... 50 2.2.8 DNA Ligation ....................................................................................................... 50 2.2.9 Preparation of Chemically Competent Cells ....................................................... 50 2.2.10 Transformation of E. coli..................................................................................... 51 2.2.11 Selection of the Positive Transformants ............................................................. 52 2.2.12 16S rDNA Sequencing ......................................................................................... 52 2.2.13 Genomic DNA Extraction, Sequencing, Assembly and Annotation .................... 53 2.2.14 Preparation of Phylogenetic Tree ....................................................................... 54 2.3 PROTEIN BIOCHEMISTRY .................................................................................... 54 2.3.1 Induction of Protein Expression and Cell-Free Extract Preparation ................... 54 2.3.2 Protein Quantification ........................................................................................ 55 2.3.3 Sodium Dodecyl Sulfate Polyacrylamide Gel Electrophoresis (SDS-PAGE) ........ 56 2.3.4 Western Blotting ................................................................................................. 57 2.3.5 Ni-NTA Purification ............................................................................................. 59 iv 2.3.6 Measurement of Myrosinase Activity by God-Perid Assay ................................ 59 2.4 CHROMATOGRAPHY METHODS .......................................................................... 61 2.4.1 High Performance Liquid Chromatography (HPLC) ............................................ 61 2.4.1.1 Preparation of sulfatase .................................................................................. 61 2.4.1.2 Desulfation of glucosinolates .........................................................................
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