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Analysis of Sequence Variation at Two Helicobacter Pylori Genetic Loci Potentially Involved in Virulence

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Analysis of Sequence Variation at Two Helicobacter Pylori Genetic Loci Potentially Involved in Virulence W&M ScholarWorks Dissertations, Theses, and Masters Projects Theses, Dissertations, & Master Projects 2008 Analysis of Sequence Variation at Two Helicobacter pylori Genetic Loci Potentially involved in Virulence George Warren Liechti College of William & Mary - Arts & Sciences Follow this and additional works at: https://scholarworks.wm.edu/etd Part of the Microbiology Commons, and the Molecular Biology Commons Recommended Citation Liechti, George Warren, "Analysis of Sequence Variation at Two Helicobacter pylori Genetic Loci Potentially involved in Virulence" (2008). Dissertations, Theses, and Masters Projects. Paper 1539626867. https://dx.doi.org/doi:10.21220/s2-zrbg-b193 This Thesis is brought to you for free and open access by the Theses, Dissertations, & Master Projects at W&M ScholarWorks. It has been accepted for inclusion in Dissertations, Theses, and Masters Projects by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. Analysis of sequence variation atHelicobacter two pylori genetic loci potentially involved in virulence. George Warren Liechti Springfield, Virginia Bachelors of Science, College of William and Mary, 2003 A Thesis presented to the Graduate Faculty of the College of William and Mary in Candidacy for the Degree of Master of Science Department of Biology The College of William and Mary May, 2008 APPROVAL PAGE This Thesis is submitted in partial fulfillment of the requirements for the degree of Master of Science George Warren Liechti Approved by^the Cq , April, 2008 Committee Chair Associate Professor Mark Forsyth, Biology, The College of William and Mary r Professor Margaret Saha, Biology, The College of William and Mary Associate Professor George Gilchrist, Biology, The College of William and Mary / J / ABSTRACT PAGE Helicobacter pylori colonizes the gastric mucosa of nearly half the world’s population and is a well documented etiologic agent of peptic ulcer disease (PUD) and a significant risk factor for the development of gastric cancer. The majority of H. pylori isolates that have been linked to peptic ulcer disease share a common genetic element known as the cag Pathogenicity Island (cag PAI). Recent studies comparing the genomes of more virulent and less virulent strains have revealed the presence of numerous pathogen-specific genes that may have been introduced to the more virulent, cag PAI positive H. pylori strains by horizontal gene transfer. In addition to the acquisition of virulence associated genes, it has been shown that gene loss also plays an important role in the development of numerous pathogens, although to date this avenue of research has been relatively unexplored in H. pylori. In this study, we show that HP1079 and HP1078, two genes of unknown function and currently lacking any orthologs in other sequenced bacterial species, exist as a co- varying locus with the cag PAI. In addition, we show that HP1079 has the potential to undergo phase variation and that HP1078 exists in two distinct allelic forms that are present in relatively equal frequencies in our study set of clinical isolates of H. pylori from North America. While a proposed role for HP1079 and HP1078 in virulence must await animal model studies, we hypothesize that this locus is a potentially novel virulence associated locus based upon its association with cag PAI positive H. pylori strains, the fact that it is subject to phase variable expression, and that one gene in this locus exhibits allelic variation. We also characterize another genetic locus, currently annotated as HP0937 and HP0938, and show that this locus appears to be actively undergoing genetic decay. The patterns of pseudogenesis are so dissimilar between isolates that we hypothesize that the selective pressure on the locus occurred subsequent to the divergence of these strains from their last common ancestor. Table of Contents List of Figures and Tables........................................................................................................vi C hapter 1. Introduction............................................................................................................1 Helicobacter pylori................................................................. 1 Infection / Colonization ........................................ 2 Bacterial Genetics........................................................................... 3 Virulence Determinants.......................................................... 5 Urease................................................................................... .....9 Motility .................................................................................................................9 Lipopolysaccharide (LPS) .......................................... 12 cag Pathogenicity Island .................................................................................. 13 Vacuolating Cytotoxin (VacA) ............................... 14 babA .............................................................. 15 The Outer Membrane Protein Adhesin, SabA.............................................. 16 oipA..................................................................................................................... 17 iceA..................................................................................................................... 18 dupA.............................................................................................................. 18 Gene Shuffling................................................................................................................18 Biofilms..........................................................................................................................19 Evolutionary Genomics................................................................................................ 20 Gene Removal: Black Holes..................................................... 21 Gene Removal : Bacteriophages.....................................................................22 Project Introduction .......... 28 Novel Virulence Determinants.................................... 28 Bacterial Pseudogene Analysis ............. 33 Chapter 2. Materials and Methodology .......................... 35 Chapter 3. Results: Allelic and Phase Variation in a cag Pathogenicity Island (PAI) Covarying Locus inHelicobacter pylori ........ .39 HP1080-1077(m'x^) Empty Site Analysis ............... 39 HP1079 and HP1078 are stable over six years within a single host. ............. .40 HP 1079 is a phase variable gene ........ 42 HP 1078 allelic variation can be divided into two types........................ 45 HP 1078 allelic variation across racial demographics................. ...................... 51 Chapter 4. Results: Identification and Analysis of a Genetic Locus Undergoing Genetic Decay Simultaneously in Divergent Strains Helicobacterof pylori....................... 56 HP0938-0937 locus shows evidence of extensive genetic decay ...................56 Chapter 5. Discussion and Future Directions....................... 61 References. .................................................................................................... 68 v List of Figures and Tables Figure 1 Identification of bacterial core genes through comparative genomics.........6 Figure 2 Analysis of the HP1078-HP1070 locus in H. pylori clinical isolates.........30 Table 1 Oligonucleotide primers used in the genetic analysis and knockout/knockin studies .............. 38 Figure 3 HP1078 is genetically stable over six years within a single host ............... 41 Figure 4 The cagA covarying gene HP 1079 is phase variable...................................43 Figure 5 The cag PAI covarying gene HP1078 exists as two major allelic variants.................................. 46 Figure 6 Allelic variation in HP 1078 among clinical isolates ........................... 49 Table 2 Distribution of HP1078 alleles...................... 52 Figure 7 HP1078 allelic variation across racial demographics...................................54 Figure 8 Comparative Analysis of the HP0938-0937 amplicon and its proposed ancestral homolog. .............. 58 INTRODUCTION Background Helicobacter pylorus is a spiral shaped, gram-negative, microaerophilic bacterium that colonizes the gastric mucosa of nearly half the world’s population. It is an etiologic agent of peptic ulcer disease (PUD) as well as a significant risk factor for the development of gastric cancer. Socio-economic status is an established indicator ofH. pylori infection rates, and in developing countries, infection rates in adults can reach as high as 90% [1,2]. Because of its prevalence in the developing world and the emergence of antibiotic resistant strains [3], research involving the classification of novelH. pylori vaccine targets and a deeper understanding of this pathogen’s interaction with its human host is of paramount importance. In this brief overview, some basic background on the pathobiology associated with infection by this organism will be examined, including its capability of eliciting disease as well as some of the environmental stresses thought to play a role in its initial and continued colonization of the human gastric mucosa. There is still considerable debate as to the mode of transmission of this bacterium. H. pylori has been cultured from stool samples of infected individuals and screening of water samples from local sources using polymerase chain reaction (PCR) methods have shown the presence of H. pylori DNA, suggesting
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