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Downloaded on 2018-08-23T19:21:15Z Title Functional genomics of commensal Lactobacilli Author(s) O'Donnell, Michelle M. Publication date 2014 Original citation O'Donnell, M. M. 2014. Functional genomics of commensal Lactobacilli. PhD Thesis, University College Cork. Type of publication Doctoral thesis Rights © 2014, Michelle M. O' Donnell http://creativecommons.org/licenses/by-nc-nd/3.0/ Item downloaded http://hdl.handle.net/10468/1558 from Downloaded on 2018-08-23T19:21:15Z FUNCTIONAL GENOMICS OF COMMENSAL LACTOBACILLI Candidate: Michelle M. O’ Donnell (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 2014 Head of Department: Prof. Gerald Fitzgerald Supervisors: Prof. R. Paul Ross and Prof. Paul W. O’ Toole Dedicated to my loving family and in memory of my father ii TABLE OF CONTENTS DECLARATION ................................................................................................................................... iv PUBLICATIONS ................................................................................................................................... v ABBREVIATIONS ................................................................................................................................. i ABSTRACT ............................................................................................................................................ ii Chapter I Catabolic flexibility of mammalian-associated lactobacilli. .............................................. 6 Chapter II Carbohydrate catabolic flexibility in the mammalian intestinal commensal Lactobacillus ruminis revealed by fermentation studies aligned to genome annotations. .............. 51 Chapter III The core faecal bacterial microbiome of Irish Thoroughbred racehorses ............... 106 Chapter IV The core microbiota of domesticated herbivorous hindgut fermenters, mono-gastric and ruminant animals ........................................................................................................................ 144 Chapter V Assessing the effect of the galactooligosaccharides and the autochthonous probiotic Lactobacillus ruminis on the pig intestinal microbiota .................................................................... 180 Chapter VI Genomic diversity and biochemical characterisation of Lactobacillus ruminis isolates of human, bovine, porcine and equine origin. .................................................................................. 217 Chapter VII The genome of the predominant equine lactobacillus species, Lactobacillus equi is reflective of its lifestyle adaptations to a herbivorous host ............................................................. 283 Chapter VIII Discussion/Conclusion ................................................................................................ 315 Acknowledgements ............................................................................................................................. 326 Appendices – Published articles ........................................................................................................ 328 iii 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. Michelle O’ Donnell _________________________________________________ iv PUBLICATIONS O’ Donnell, M. M., Forde, B. M., Neville, B. A., Ross, R. P. and O’ Toole, P. W. Carbohydrate catabolic flexibility in the mammalian intestinal commensal Lactobacillus ruminis revealed by fermentation studies aligned to genome annotations. Microbial Cell Factories, 10, Suppl 1 2011), S12. O' Donnell, M. M., O' Toole, P. W. and Ross, R. P. Catabolic flexibility of mammalian-associated lactobacilli. Microbial Cell Factories, 12, 1 2013), 48. O' Donnell, M. M., Harris, H. M. B, Jeffery, I. B., Claesson, M. J., Younge, B., O' Toole, P. W. and Ross, R. P. The core faecal bacterial microbiome of Irish Thoroughbred racehorses. Letters in Applied Microbiology, 57, 6, 2013), 492-501. O’ Donnell, M. M., Harris, H. M. B., O’ Toole P. W. and Ross, R. P. The genome of the predominant equine lactobacillus species, Lactobacillus equi is reflective of its lifestyle adaptations to a herbivorous host. Genome Announcements, 2, 1, 2014). O’ Donnell, M. M., Harris, H. M. B., Ross, R. P. and O’ Toole P. W. The core microbiota of domesticated herbivorous hindgut fermenters, mono- gastric and ruminant animals. In preparation as research article intended for submission to PLOS One. O’ Donnell, M. M., Harris, H. M. B., Lynch, D., Ross, R. P. and O’ Toole P. W. Genomic diversity and biochemical characterisation of Lactobacillus ruminis isolates of human, bovine, porcine and equine origin. In preparation as research article intended for submission to Applied Environmental Microbiology. O’ Donnell, M. M., Harris, H. M. B., Lakshminarayanan, B., Lawlor, P. G., O’ Toole P. W. and Ross, R. P. Assessing the effect of the galactooligosaccharides and the autochthonous probiotic Lactobacillus ruminis on the pig intestinal microbiota. In preparation as a research article for submission to Letters in Applied Microbiology. v ABBREVIATIONS AA = Amino Acid ACT = Artemis Comparison Tool BLAST = Basic Local Alignment Search Tool BSH = Bile Salt Hydrolase cDNA = Complementary DNA CDS = Coding DNA Sequence cfMRS = Carbohydrate-free MRS COG = Clusters of Orthologous Groups CFU = Colony Forming Units DGGE = Denaturing Gel Gradient Electrophoresis EDTA = Ethylene-diamine-tetraacetic acid EFSA = European Food Safety Authority EPS = Exopolysaccharide EST = Expressed Sequence Tag FAO/WHO = Food and Agriculture Organisation of the United Nations and the World Health Organisation FOS = Fructooligosaccharide GAPDH = Glyceraldehyde 3 Phosphate Dehydrogenase GI = Gastrointestinal GOS = Galactooligosaccharide GRAS = Generally Regarded As Safe HMP = Human Microbiome Project KAAS = KEGG Automatic Annotation Server KEGG = Kyoto Encyclopedia of Genes and Genomes LAB = Lactic Acid Bacteria LPS = Lipopolysaccharide MCP = Methyl accepting chemotaxis protein MRS = de Mann-Rogosa-Sharpe NCBI = National Center for Biotechnology Information NF- κB = Nuclear Factor κ B NGS = Next-generation Sequencing NT = Nucleotide ORF = Open Reading Frame OTU = Operational Taxonomic Unit PCR = Polymerase Chain Reaction qRT-PCR = Quantitative Real-Time PCR QTL = Quantitative Trait Locus RACE = Rapid Amplification of cDNA Ends RBS = Ribosome Binding Site RFLP = Restriction Fragment Length Polymorphism rRNA = Ribosomal RNA SCFA = Short Chain Fatty Acid SOS = Soybean-oligosaccharide S. typhimurium = Salmonella enterica serovar Typhimurium T-RFLP = Terminal Restriction Fragment Length Polymorphism ABSTRACT ii Catabolic flexibility affords a bacterium the ability to utilise various sugars as carbon sources for energy. This ability is particularly important for commensal lactobacilli which are exposed to a variety of simple and complex carbohydrates in vivo. Lactobacillus ruminis has been identified as one of a limited number of truly autochthonous commensal lactobacilli identified in the gastrointestinal tract of humans and other mammals. However, little was known at the outset of this thesis research about the fermentation capabilities and metabolic pathways used by L. ruminis that allow it to survive in vivo. Chapter 1 provides a detailed literature perspective and context on the various catabolic flexibility mechanisms utilised by other mammalian associated lactobacilli to enable them to survive in the gastrointestinal tracts of their hosts. A combination of in vitro and in silico techniques was used to identify the pathways, enzymes and transporters involved in the utilisation of a variety of carbohydrates by L. ruminis. The transport and catabolic machinery involved in the utilization of ≥50 carbohydrates including prebiotics were identified by comparison of in vitro fermentation profiles with the genome annotation of two L. ruminis strains (ATCC 25644 and ATCC 27782). Prebiotic utilisation operons and transporters were identified in silico. Carbohydrate symporter transport families were identified as the primary transporters of relatively complex carbohydrates in L. ruminis. In contrast, simpler carbohydrates like mono and di-saccharide sugars were transported via energy dependent transport systems. This suggested that L. ruminis has adapted to its intestinal niche which provides a steady supply of carbon sources that allows L. ruminis to use less energy dependent methods of carbohydrate translocation. Microbiota dysbiosis-related diseases may be caused or aggravated by the ingestion of certain carbohydrates. Diet is a major factor that affects the bacterial diversity of the gut microbiota. To help prevent gut-related health loss in important animals, such as racehorses and other performance animals, it is important to identify the core microbiota of healthy animals consuming different feeds. Culture- independent analysis of the microbiota of six healthy racehorses revealed that the core microbiota of these hindgut animals was dominated by the Firmicutes and Bacteroidetes phyla. While not the main focus of the study, differences between the groups were noted. Active horses receiving high starch concentrate feed had lower microbiota diversity than naturally grazing horses at rest. This loss of diversity iii coincided with an increase in the abundance
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