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Staphylococcus Aureus in Australia and New Zealand Evolutionary Dynamics of Successful Clones of Methicillin-Resistant Staphylococcus aureus in Australia and New Zealand Sarah Louise Baines MSc BMLSc ORCID: 0000-0002-0557-0518 Doctor of Philosophy October 2019 Department of Microbiology & Immunology, The University of Melbourne at The Peter Doherty Institute for Infection & Immunity Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy I Abstract Staphylococcus aureus is a common cause of bacterial infections in humans and a leading nosocomial pathogen, associated with significant morbidity, mortality and economic impact. A cornerstone in the evolution of staphylococcal lineages that infect humans has been their remarkable ability to rapidly and efficiently develop or acquire mechanisms of antimicrobial resistance, impacting effective disease management, prevention, and eradication. Improving these measures or developing novel approaches requires a comprehensive understanding of the infecting agent and while S. aureus has been extensively studied there remains considerable gaps in our knowledge surrounding this pathogen, especially concerning population dynamics. What drives the emergence and/or persistence of certain staphylococcal lineages? What evolutionary pathways and molecular mechanisms are being utilised and under what circumstances? What environmental and host factors have the greatness influence on bacterial population adaptation? And ultimately, what are the consequence of these population level changes and what impact do these have on staphylococcal disease? This thesis represents three projects undertaken to strengthen our understanding of the evolutionary dynamics surrounding staphylococcal population adaptation, using a combination of comparative genomics and detailed phenotypic profiling to provide insight into antibiotic-resistant lineages of S. aureus that circulate in Australia and New Zealand. The first project investigated the long-term persistence of the globally disseminated, multidrug resistant hospital-associated methicillin-resistant S. aureus (MRSA) lineage ST239 in Australia. From this work, it has been identified that the ST239 MRSA population circulating in Australia represents not one, but two genetically distinct clades; the previously unrecognised introduction of the Asian-Australian clade followed by successful local expansion in the state of Victoria has contributed to the persistence of ST239 by supplementing the diminishing population size of the local clone, the Australian clade. The ability of the Asian-Australian clade to spread following its introduction is owed to the reduced susceptibility this population developed against anti-MRSA antibiotics, namely the glycopeptides and daptomycin, prior to its importation. This same phenotype has convergently emerged in the local Australian clade. However, this adaption has come at a cost as both clades were found to have reduced replicative fitness and impaired pathogenic potential, the latter occurring through loss of functionality or reduced expression of a staphylococcal global virulence regulatory system, the accessory gene regulator. The second project considered a different evolutionary circumstance; the rapid emergence of a novel MRSA lineage in the New Zealand community. This region has a high incidence of staphylococcal skin and soft tissue infection and over the last two decades has seen a significant shift in the local molecular epidemiology of S. aureus, with the emergence of multiple fusidic acid resistant clones. This work has focused on the predominant MRSA lineage, an ST5 clone locally referred to as AK3. Genomic investigation of this lineage has found that II AK3 represents a single phylogenetic clade that has arisen through local population expansion, having emerged from a resident fusidic acid susceptible methicillin-susceptible S. aureus upon the acquisition of a novel chimeric SCCmecIVa-fusC II mobile element harbouring the fusidic acid resistance determinant fusC. This phenomenon was not restricted to ST5, with the other newly emerged lineages having acquired fusC via structurally distinct SCC and SCCmec elements. Indicating that, the unregulated use of fusidic acid in the region has supported the emergence and expansion of these novel lineages and is potentially contributing to the high local incidence of staphylococcal infection. Mobile elements can greatly influence staphylococcal populations, therefore the third project focused on exploring the evolution of the multidrug resistant plasmid family pSK1 and the role it has played in augmenting antimicrobial resistance and biocide tolerance in the ST239 MRSA population in Australia. Modelling the evolutionary history of this plasmid identified that it emerged during the late 1970s and over the following four decades has undergone significant structural change, involving a combination of chromosomal integration, transposon loss/gain, structural inversion and deletion events. When aligned to a phylogenetic model of the ST239 population, it became apparent that these changes in plasmid configuration represented a clear pathway of step-wise adaptation; the shortened, chromosomally integrated plasmid structural variants having emerged on multiple occasions in a convergent manner. Further, these changes correlated with the development of enhanced tolerance against chlorhexidine, an important finding as it implicates biocide use as a factor potentially influencing MRSA evolution. Collectively, this work enhances our understanding of how antibiotic-resistant lineages of S. aureus evolve and adapt; exemplifying the evolutionary pathways facilitating adaptation in staphylococcal populations and the circumstances under which they are used. Further, it provides detailed insight into two highly successful lineages of MRSA. This knowledge can be exploited to improve measures that reduce the burden of antibiotic-resistant staphylococcal infection. Importantly, this work enhances and reinforces our awareness about the consequences of antimicrobial overuse and misuse. III Declaration This is to certify that: I. This thesis, entitled “Evolutionary Dynamics of Successful Clones of Methicillin-Resistant Staphylococcus aureus in Australia and New Zealand”, comprises only my original work towards this Ph.D except where otherwise indicated; II. Due acknowledgement has been made in the text to all other material used; III. The thesis is fewer than 100,000 words in length, exclusive of tables, figures, figure legends, bibliography, and appendices. ........................................................ Sarah Louise Baines MSc BMLSc Department of Microbiology & Immunology The University of Melbourne at The Peter Doherty Institute for Infection & Immunity IV Preface This preface provides a summary of the contents of each chapter in this thesis. The chapters that include publications are indicated. The nature and extent of the contributions to each chapter made by the author of this thesis are listed. Funding: Sarah Louise Baines was supported by an Australian Government Research Training Program Scholarship. Additional funding was awarded in the form of a Victorian Fellowship, provided by the Victoria State Government to undertake an overseas study mission. This supported the research presented in this thesis and unpublished projects representing extensions of this work. Funding awarded to co-authors of the publications presented in this thesis are indicated below. Chapter 1: Introduction is an original overview of the background, key concepts and motivations for this thesis, with the original works cited. Chapter 2: Convergent Adaptation in the Dominant Global Hospital Clone ST239 of Methicillin-Resistant Staphylococcus aureus is an original work that resulted in the following publication: Baines, S. L., K. E. Holt, M. B. Schultz, T. Seemann, B. O. Howden, S. O. Jensen, S. J. van Hal, G. W. Coombs, N. Firth, D. R. Powell, T. P. Stinear and B. P. Howden (2015). "Convergent adaptation in the dominant global hospital clone ST239 of methicillin-resistant Staphylococcus aureus." MBio; DOI: 10.1128/mBio.00080-15. The author of this thesis was the first author and main contributor of the work presented in this publication. The nature and extent of my contributions to this chapter are described below. • I contributed to the generation of data (exceptions listed below), interpretation of results, and development of the concepts described in the publication with BPH and TPS. • I generated all new sequence data presented in this publication. Several bacterial isolates and/or whole genome sequence data was kindly provided by SOJ, SJH and NF. • I performed all bioinformatics analyses, except for recombination detection which was performed by KEH. Supervision, teaching and/or software was provided by TPS, TS, KEH, MBS and DRP. • I performed all phenotypic experiments. Assistance with a murine sepsis model was provided by BOH. All animal studies were performed in accordance with the Animal Research Ethics Committee at The University of Melbourne (Ethics Application #1212591). V • I was responsible for the planning, drafting, and editing of the publication with BPH and TPS. • All co-authors reviewed and edited the manuscript. Funding associated with this publication include National Health and Medical Research Council, Australia: Fellowships awarded to BPH (APP1023526), TPS (APP1008549), and KEH (APP1061409). Chapter 3: Rapid Emergence and Evolution of Staphylococcus aureus Clones Harbouring fusC-Containing Staphylococcal
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