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Downloaded on 2017-02-12T04:29:14Z Title Functional genomics of motile commensal intestinal bacteria Author(s) Neville, B. Anne Publication date 2013 Original citation Neville, B. A. 2013. Functional genomics of motile commensal intestinal bacteria. PhD Thesis, University College Cork. Type of publication Doctoral thesis Rights © 2013. Anne Neville http://creativecommons.org/licenses/by-nc-nd/3.0/ Embargo information Please note that Appendix A & B are currently unavailable due to a restriction requested by the author. Embargo lift date 10000-01-01 Item downloaded http://hdl.handle.net/10468/1201 from Downloaded on 2017-02-12T04:29:14Z FUNCTIONAL GENOMICS of MOTILE COMMENSAL INTESTINAL BACTERIA Candidate: B. Anne Neville (BSc) A thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy. Department of Microbiology, National University of Ireland, Cork, Ireland. January 2013 Supervisors: Prof. Paul W. O’Toole & Prof. R. Paul Ross Examiners: Dr. Anne McCartney (External) & Prof. Douwe van Sinderen (Internal) Head of Dept.: Prof. Gerald Fitzgerald 1 Declaration I hereby declare that the content of this thesis is the result of my own work and has not been submitted for another degree, either at University College Cork or elsewhere. ___________________________________ B. Anne Neville 2 This thesis is dedicated to my family. 3 General Table of Contents Table of Figures…………………………………………………………5 Table of Tables……………………………………….………………….7 Abbreviations……………………………………………………………9 Abstract……………………………………………………………...…13 Chapter 1: General Introduction…….………….…….………..……16 Chapter 2: Characterization of pro-inflammatory flagellin proteins produced by Lactobacillus ruminis and related motile lactobacilli………………………...…………………………..………117 Chapter 3: Pro-inflammatory flagellins from abundant motile commensal bacteria are variably represented in the intestinal microbiomes of elderly humans………………………….……….…189 Chapter 4: General Discussion……………..………...……………..257 Appendix A: Probiotic properties of Lactobacillus salivarius and closely related Lactobacillus species (Published article)........……...277 Appendix B: Genomics (Accepted for publication)………………..325 Acknowledgements…………………………………………………...398 4 Table of Figures Figure 1.1: Anatomy and Lactobacillus communities of the human gastrointestinal tract. ............................................................................. 23 Figure 1.2: Structural differences between basal-bodies of Gram positive and Gram negative bacteria. .................................................. 58 Figure 1.3: Structure of a flagellin monomer and the flagellar filament. .................................................................................................. 61 Figure 1.4: Flagellin induced TLR5 signalling pathway. .................. 74 Figure 2.1: Transmission electron micrographs of L. ruminis whole cells and flagella. .................................................................................. 128 Figure 2.2: Extraction of Lactobacillus flagellin proteins and analysis on 10% SDS-PAGE gels. ..................................................................... 133 Figure 2.3: Flagellate L. ruminis cells or Lactobacillus flagellin stimulate IL8 production by intestinal epithelial cells in a TLR5- dependent manner. .............................................................................. 135 Figure S2.1: Genetic organization of the L. ruminis ATCC27782 motility locus......................................................................................... 165 Figure S2.2: Artemis Comparison Tool (ACT) alignment of L. ruminis ATCC27782 and L. mali DSM20444T motility loci ............. 166 Figure S2.3: 16S rRNA gene tree and motility protein based phylogenetic trees. ................................................................................ 174 Figure S2.4: Proposed model for regulation of flagellum biogenesis. ................................................................................................................ 175 Figure S2.5: Characterization of the immune responses induced by native and recombinant Lactobacillus flagellin proteins in epithelial cell lines. ................................................................................................ 176 Figure S2.6: Failure of altered growth media to impart motility to L. ruminis ATCC25644 on semi-solid agar plates ................................. 177 Figure 3.1: Gene order plot of major motility gene loci in Eubacterium and Roseburia genomes ................................................. 199 Figure 3.2: Flagellin proteins from E. rectale and R. inulinivorans separated on Coomassie stained SDS-PAGE gels. ............................ 202 5 Figure 3.3: Mutliple alignment of the consensus region of the flagellin proteins of β and γ proteobacteria that is recognised via TLR5 with the corresponding regions of predicted flagellin proteins from the Roseburia and Eubacterium species studied ...................... 207 Figure 3.4: IL-8 secretion from T84 cells (A) and HT-29 cells (B) in response to flagellin preparations from E. rectale and R. inulinivorans ................................................................................................................ 209 Figure S3.1: ACT alignments of flgB-fliA (top) and flgM-flgN/fliC (bottom) motility loci ........................................................................... 236 Figure S3.2: Phylogenetic tree of flagellin proteins ......................... 237 Figure S3.3: Heat-plots showing the relationship between the normalized number of reads mapped to target motility CDSs as a function of CDS length and target species relative abundance. ...... 243 Figure S3.4: Recruitment plots demonstrating the presence or absence of the flagellin proteins of interest in 27 metagenomes. ..... 246 Figure A 1: Summary of the species in the L. salivarius clade and the general sources from which they were first isolated. ....................... 280 Figure A 2: Adhesion of sortase dependent proteins to cell wall of Gram positive bacteria. ....................................................................... 302 Figure B 1: Genetic organisation of a typical LAB plasmid - L. lactis subsp. cremoris plasmid pSK11L. ...................................................... 341 Annex B 1: Interpretation of a genome atlas. .................................. 347 Annex B 2: Visualization of whole genome alignments to assess overall sequence and organizational similarity................................. 349 6 Table of Tables Table 1.1: Cellular location and ligands of Toll like receptors ........ 43 Table 1.2: Flagella distribution patterns ........................................... 53 Table 1.3: Modes of bacterial motility ................................................ 54 Table 1.4: Profile of human TLR5 gene expression in various body sites as inferred from EST and cDNA library sources. ...................... 69 Table S2.1: Origin and phylogeny of motile Lactobacillus species described to date .................................................................................. 178 Table S2.2: Lactobacillus strains and species used in this study ..... 179 Table S2.3: Closest homologs* of L. ruminis motility proteins ....... 180 Table S2.4: Expression analysis of flagellum biogenesis and chemotaxis genes in L. ruminis derived by type I microarray. ....... 182 Table S2.5: Primers used in this study .............................................. 183 Table S2.6: Uniprot and NCBI accession numbers for motility proteins .................................................................................................. 184 Table 3.1: Summary of the properties of Eubacterium and Roseburia flagellin proteins and their predicted promoter and ribosome binding site sequences ........................................................................................ 203 Table S3.1: Locus tags for motility loci from genomes of interest. 247 Table S3.2: Amino-terminal sequences of E. rectale A1-86 and R. inulinivorans A2-194 flagellin proteins. ............................................. 249 Table S3.3: Relative abundance (%) of each target species in 25 of the shotgun metagenomes of interest, as calculated by MetaPhlAn. ................................................................................................................ 250 Table S3.4: Estimated target genome coverage in each metagenome. ................................................................................................................ 251 Table S3.5: Summary of the number of ORFs per metagenome identified as a motility gene or gene fragment from a species of interest. .................................................................................................. 254 7 Table S3.6: “Cell Motility” COG category analysis for assembled metagenomes. ....................................................................................... 255 Table S3.7: Strains and Genomes used in this study. ...................... 256 Table A 1: Species of the L. salivarius phylogenetic clade. ............. 281 Table A 2: Checklist summarizing the probiotic evaluation of L. salivarius UCC118. ............................................................................... 283 Table B 1: Summary of the first genome project for each Lactobacillus species sequenced to date (July 2012). ........................ 337 8 Abbreviations AA = Amino Acid ACT = Artemis Comparison Tool ACTB = β-actin ANI = Average Nucleotide Identity BCA = Bicinchoninic Acid BLAST = Basic
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