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MORPHOLOGIC AND GENOMIC CHARACTERISATION OF THE KOALA CHLAMYDIA PNEUMONIAE STRAIN Candice Melissa Mitchell Bachelor of Applied Science (Honours I), QUT 2006 Institute of Health and Biomedical Innovation School of Life Sciences Queensland University of Technology Brisbane, Australia A thesis submitted for the degree of Doctor of Philosophy of the Queensland University of Technology 2010 ii LIST OF KEYWORDS Chlamydia pneumoniae; Chlamydia; pathogen; respiratory; characterisation; developmental cycle; elementary body; reticulate body; inclusion morphology; genome; genomic comparison; bioinformatics; single nucleotide polymorphism; SNP; PCR; gene sequencing. iii ABSTRACT Chlamydia pneumoniae is a common human and animal pathogen associated with a wide range of upper and lower respiratory tract infections. In more recent years there has been increasing evidence to suggest a link between C. pneumoniae and chronic diseases in humans, including atherosclerosis, stroke and Alzheimer’s disease. C. pneumoniae human strains show little genetic variation, indicating that the human-derived strain originated from a common ancestor in the recent past. Despite extensive information on the genetics and morphology processes of the human strain, knowledge concerning many other hosts (including marsupials, amphibians, reptiles and equines) remains virtually unexplored. The koala (Phascolarctos cinereus) is a native Australian marsupial under threat due to habitat loss, predation and disease. Koalas are very susceptible to chlamydial infections, most commonly affecting the conjunctiva, urogenital tract and/or respiratory tract. To address this gap in the literature, the present study (i) provides a detailed description of the morphologic and genomic architecture of the C. pneumoniae koala (and human) strain, and shows that the koala strain is microscopically, developmentally and genetically distinct from the C. pneumoniae human strain, and (ii) examines the genetic relationship of geographically diverse C. pneumoniae isolates from human, marsupial, amphibian, reptilian and equine hosts, and identifies two distinct lineages that have arisen from animal-to-human cross species transmissions. Chapter One of this thesis explores the scientific problem and aims of this study, while Chapter Two provides a detailed literature review of the background in this field of work. Chapter Three, the first results chapter, describes the morphology and developmental stages of C. pneumoniae koala isolate LPCoLN, as revealed by fluorescence and transmission electron microscopy. The profile of this isolate, when cultured in HEp-2 human epithelial cells, was quite different to the human iv AR39 isolate. Koala LPCoLN inclusions were larger; the elementary bodies did not have the characteristic pear-shaped appearance, and the developmental cycle was completed within a shorter period of time (as confirmed by quantitative real-time PCR). These in vitro findings might reflect biological differences between koala LPCoLN and human AR39 in vivo. Chapter Four describes the complete genome sequence of the koala respiratory pathogen, C. pneumoniae LPCoLN. This is the first animal isolate of C. pneumoniae to be fully-sequenced. The genome sequence provides new insights into genomic ‘plasticity’ (organisation), evolution and biology of koala LPCoLN, relative to four complete C. pneumoniae human genomes (AR39, CWL029, J138 and TW183). Koala LPCoLN contains a plasmid that is not shared with any of the human isolates, there is evidence of gene loss in nucleotide salvage pathways, and there are 10 hot spot genomic regions of variation that were previously not identified in the C. pneumoniae human genomes. Sequence (partial-length) from a second, independent, wild koala isolate (EBB) at several gene loci confirmed that the koala LPCoLN isolate was representative of a koala C. pneumoniae strain. The combined sequence data provides evidence that the C. pneumoniae animal (koala LPCoLN) genome is ancestral to the C. pneumoniae human genomes and that human infections may have originated from zoonotic infections. Chapter Five examines key genome components of the five C. pneumoniae genomes in more detail. This analysis reveals genomic features that are shared by and/or contribute to the broad ecological adaptability and evolution of C. pneumoniae. This analysis resulted in the identification of 65 gene sequences for further analysis of intraspecific variation, and revealed some interesting differences, including fragmentation, truncation and gene decay (loss of redundant ancestral traits). This study provides valuable insights into metabolic v diversity, adaptation and evolution of C. pneumoniae. Chapter Six utilises a subset of 23 target genes identified from the previous genomic comparisons and makes a significant contribution to our understanding of genetic variability among C. pneumoniae human (11) and animal (6 amphibian, 5 reptilian, 1 equine and 7 marsupial hosts) isolates. It has been shown that the animal isolates are genetically diverse, unlike the human isolates that are virtually clonal. More convincing evidence that C. pneumoniae originated in animals and recently (in the last few hundred thousand years) crossed host species to infect humans is provided in this study. It is proposed that two animal-to-human cross species events have occurred in the context of the results, one evident by the nearly clonal human genotype circulating in the world today, and the other by a more animal-like genotype apparent in Indigenous Australians. Taken together, these data indicate that the C. pneumoniae koala LPCoLN isolate has morphologic and genomic characteristics that are distinct from the human isolates. These differences may affect the survival and activity of the C. pneumoniae koala pathogen in its natural host, in vivo. This study, by utilising the genetic diversity of C. pneumoniae, identified new genetic markers for distinguishing human and animal isolates. However, not all C. pneumoniae isolates were genetically diverse; in fact, several isolates were highly conserved, if not identical in sequence (i.e. Australian marsupials) emphasising that at some stage in the evolution of this pathogen, there has been an adaptation/s to a particular host, providing some stability in the genome. The outcomes of this study by experimental and bioinformatic approaches have significantly enhanced our knowledge of the biology of this pathogen and will advance opportunities for the investigation of novel vaccine targets, antimicrobial therapy, or blocking of pathogenic pathways. vi LIST OF PUBLICATIONS AND MANUSCRIPTS The following is a list of publications and manuscripts that have been prepared in conjunction with this thesis. MitchellU CM,U Mathews SA, Theodoropoulos C and Timms P (2009). In vitro characterisation of koala Chlamydia pneumoniae: morphology, inclusion development and doubling time. Veterinary Microbiology. 136, 91-99. Myers GSA, Mathews SA, Eppinger M, MitchellU C,U O’Brien KK, White OR, Benahmed F, Brunham RC, Read TD, Ravel J, Bavoil PM and Timms P (2009). Evidence that human Chlamydia pneumoniae was zoonotically acquired. Journal of Bacteriology. 191, 7225-7233. MitchellU CM, U Hovis KM, Bavoil P, Myers GSA, Carrasco JA and Timms P (2010). Comparative genomics of Chlamydia pneumoniae of human and animal origins highlights genetic diversity in the species. BMC Genomics. (Submitted with revisions, February 2010). MitchellU CM, U Hutton S, Myers GSA, Brunham R and Timms P (2010). Chlamydia pneumoniae is genetically diverse in animals and appears to have crossed the host barrier to humans on (at least) two occasions. PLoS Pathogens. (In Press). vii THESIS-ASSOCIATED ABSTRACTS AND PRESENTATIONS Invited Speaker: MitchellU CM U and Timms P (2008). Chlamydial infections in koalas. Wildlife animals and careers day, Currumbin Wildlife Sanctuary, Currumbin, Australia. MitchellU CM U and Timms P (2008). Genomic and morphological characterisation of the koala strain of Chlamydia pneumoniae. Harvard Medical School, Boston, United States. Oral Presentations: MitchellU CM U and Timms P (2008). Koala (LPCoLN) Chlamydia pneumoniae: A genetic and morphological characterisation. IHBI inspires conference, Gold Coast, Australia. MitchellU CM, U Mathews S and Timms P (2007). Analysis of the koala Chlamydia strain. Second Australian International Chlamydia Conference, Brisbane, Australia. Poster presentations: MitchellU CM, U Myers GSA and Timms P (2009). Koala Chlamydia pneumoniae: Evolutionary insights into the MAC/perforin. Complement, perforins and bacterial CDCs: The hole family, Prato, Italy. MitchellU CM, U Mathews SA, Theodoropoulos C, Myers GSA and Timms P (2008). Morphological and comparative genomic analysis of koala Chlamydia viii pneumoniae. Wildlife animals and careers day, Currumbin Wildlife Sanctuary, Currumbin, Australia. MitchellU CM, U Mathews SA, Theodoropoulos C, Myers GSA and Timms P (2008). Characterisation of koala Chlamydia pneumoniae: Genetic and morphological analysis. 108th American Society for Microbiology general meeting, Boston, United States. MitchellU CM, U Mathews SA, Theodoropoulos C, Myers GSA and Timms P (2007). Morphological and comparative genomic analysis of koala Chlamydia pneumoniae. The International Conference on Genome Informatics (GIW), Gold Coast, Australia. MitchellU CM, U Mathews SA, Theodoropoulos C, Myers GSA and Timms P (2007). Morphological and comparative genomic analysis of koala Chlamydia pneumoniae. IHBI inspires conference, Brisbane,
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