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Molecular Typing and Evolutionary Relationships of Salmonella Enterica Serovar Typhi

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Molecular Typing and Evolutionary Relationships of Salmonella Enterica Serovar Typhi Molecular typing and evolutionary relationships of Salmonella enterica serovar Typhi Sophie Octavia School of Biotechnology and Biomolecular Sciences The University of New South Wales Australia A thesis submitted for the degree of Doctor of Philosophy March 2008 PLEASE TYPE 1.3.1 THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Octavia First name: Sophie Other name/s: PhD in Microbiology Abbreviation for degree as given in the University calendar: School: Biotechnology and Biomolecular Sciences Faculty: Science Title: Molecular typing and evolutionary relationships of Salmonella enterica serovar Typhi Abstract 350 words maximum: (PLEASE TYPE) The evolutionary relationship between Salmonella enterica serovar Typhi, other typhoid-like enteric fever causing serovars and 10 non- Typhoid serovars from S. enterica subspecies I, could not be determined by comparative nucleotide sequences of six genes. Phylogenetic analyses of the dataset showed that the genes of interest underwent frequent recombination, suggesting a low level of clonality within subspecies I of S. enterica. To establish the evolutionary relationships within serovar Typhi, genome-wide Single Nucleotide Polymorphism (SNP) was explored as a marker for both typing purposes and phylogenetic analysis. Thirty eight SNPs were typed in 73 global Typhi isolates, including 18 isolates expressing the special flagellar antigen z66, using restriction enzyme digestion method. The isolates were differentiated into 23 SNP profiles and grouped into four distinct clusters. The z66 isolates were divided into four SNP profiles and were all grouped into one cluster, suggesting a single origin. An alternative SNP typing method using the hairpin real time PCR assay was investigated to type four additional SNPs, termed as biallelic polymorphisms (BiP). These BiPs were found to classify 481 global Typhi isolates into five major clusters (Roumagnac et al., 2006). Typing four BiPs resulted in the identification of four additional SNP profiles. We proposed nine SNPs were required to type Typhi isolates into 13 subclusters for global epidemiology. An enzymatic-based method using CelI nuclease was evaluated to discover more SNPs from other Typhi genomes. The efficiency of the CelI was shown to be unsatisfactory and we were unable to demonstrate the effectiveness of the proposed method. Nine Variable Number of Tandem Repeats (VNTRs) were typed in the 73 Typhi isolates using fluorescent-labelled universal primers, and analysed on an automated DNA sequencer. Five isolates were unable to give PCR products in one or more VNTR loci. Nine VNTRs could differentiate 68 Typhi isolates into 65 MLVA profiles, suggesting a higher discriminating power than SNP typing. SNPs were shown to be a more appropriate marker for phylogenetic tracing for Typhi while VNTRs were highly discriminating but could not be used to establish the evolutionary relationships of diverse Typhi isolates.. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). …………………………………………………………… ……………………………………..……………… ……….……………………...…….… Signature Witness Date The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: 1.4 THIS SHEET IS TO BE GLUED TO THE INSIDE FRONT COVER OF THE THESIS I Originality statement ‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’ Signed …………………………………………….............. Date …………………………………………….............. I Acknowledgement I would like to thank my supervisor, Dr. Ruiting Lan, for his invaluable advice, infinite patience and continuous guidance since my PhD year. I also would like to thank my PhD committees, Prof. Hazel Mitchell and Dr. Mark Tanaka, for their constructive feedback and comments during my PhD progress reviews. I would like to thank members of Evolutionary Microbiology Lab and all the people in Lab 301 (Helicobacter and Campylobacter Research Lab and Epsilon Proteobacteria Lab) for making the lab enjoyable. Special thanks to Alfred for being a considerate, resourceful and entertaining neighbour both in the lab and in the office. Thank you to the 2007 Honours Students (Kyi, Nat and Stan) for an extremely fun year. I am very grateful to the proofreaders (Alvin, Arash, Connie, Garry, Krisa, Luis, Nadeem, Phebe, Ram, Reg, Stan and Winnie) of my thesis (voluntarily and involuntarily); my friends, for “all the best” wishes, prayers and believing in me; and last but not least to my family for their continuous moral supports, a big thank you to my loving and understanding parents who regularly provide me nutritious meals. This thesis is dedicated to you! “I can do all things through Christ who strengthens me.” Phil 4:13 II Abstract Salmonella enterica serovar Typhi (simply referred to as Typhi) causes typhoid fever, a serious systemic infection spread by the faecal-oral route. This thesis investigated the relationships of Typhi to other serovars belonging to S. enterica subspecies I and between isolates within the Typhi clone. Initial attempt was made to determine the evolutionary relationship between Typhi and the other typhoid-like enteric fever causing serovars including serovars Paratyphi A, Paratyphi B clone b1, Paratyphi C and Sendai. The nucleotide sequences of six genes were analysed in these serovars (excluding Sendai) as well as in 10 non-typhoid serovars from S. enterica subspecies I. The relationships between the serovars were unable to be established as the phylogenetic analyses of the dataset showed that the genes studied underwent frequent recombination. This suggested a low level of clonality within subspecies I of S. enterica and this new finding has challenged the current notion that S. enterica is highly clonal. Current DNA-based typing methods such as pulse field gel electrophoresis and ribotyping are not useful to establish the evolutionary relationships of Typhi. Population structure studies using Multilocus Enzyme Electrophoresis and Multilocus Sequence Typing (MLST) have shown that Typhi is highly homogeneous. For epidemiological investigation and understanding the evolution of the pathogen, a method that can fulfil both purposes will be ideal. Therefore, genome-wide Single Nucleotide Polymorphism (SNP) was explored as a marker for both typing purposes and phylogenetic analysis. The comparison of two complete genomes for serovar Typhi strains Ty2 and CT18 allowed 38 SNPs to be selected and these were typed using restriction enzyme digestion. Seventy-three isolates from around the world, isolated between 1981-1995, were SNP-typed. They were differentiated into 23 SNP profiles, 12 profiles were represented by a single isolate and 11 profiles were shared by more than one isolate. The overall relationships of these SNP profiles were visualised using a minimum spanning network. The relationships of most SNP profiles could be resolved and these profiles divided into four major clusters, cluster I to cluster IV. We have shown III that SNPs were useful markers for establishing the relationships of Typhi isolates and were more discriminating than MLST. The 18 isolates expressing the z66 flagellar antigen included in the study were divided into four SNP profiles. These SNP profiles were grouped into one cluster, suggesting a single origin. Our evolutionary analysis suggested that Typhi was originally monophasic having only an H1 antigen and then gained a new phase-2-flagellin like operon only recently. An alternative SNP typing method using the hairpin real time PCR assay was investigated to type four additional SNPs. These SNPs, termed as biallelic polymorphisms (BiP), were found by Roumagnac et al. (2006, Science 314:1301-1304) to classify global Typhi isolates into five major clusters. These BiPs, BiP 36, BiP 48, BiP 56 and BiP 33, were selected to type the 73 Typhi isolates used in this study. Two BiPs, BiP 36 and 33, were found to be unique in one isolate each. Typing four BiPs resulted
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