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Legionella Pneumophila Biofilm Formation, Environmental Dissemination and Pathogenicity

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Legionella Pneumophila Biofilm Formation, Environmental Dissemination and Pathogenicity The Role of the Legionella Collagen-Like Protein in Legionella pneumophila Biofilm Formation, Environmental Dissemination and Pathogenicity by Mena Abdel-Nour A thesis submitted in conformity with the requirements for the degree of Masters of Science Department of Laboratory Medicine and Pathobiology University of Toronto © Copyright Mena Abdel-Nour (2013) The Role of the Legionella Collagen-Like Protein in Legionella pneumophila Biofilm Formation, Environmental Dissemination and Pathogenicity Mena Abdel-Nour Masters of Science Department of Laboratory Medicine and Pathobiology University of Toronto 2013 Abstract The Legionella collagen-like protein (Lcl) of Legionella pneumophila is an adhesin involved in multiple processes during the lifecycle of L. pneumophila. Among these processes is the sedimentation and auto-aggregation of L. pneumophila. Lcl potentiates the infection of amoeba species by facilitating contact and adhesion to its host, allowing the pathogen to replicate, disseminate and persist in the environment. Lcl dependent auto- aggregation requires divalent cations, suggesting it may occur in the natural habitat of L. pneumophila. In addition to its role in sedimentation, Lcl mediates biofilm production of L. pneumophila. The Lcl encoding gene, lpg2644 is polymorphic among clinical isolates, and the number of collagenous repeats is positively correlated to biofilm production and clinical prevalence. This study underscores the role of Lcl in human infection by contributing to environmental dissemination and persistence, thereby increasing the likelihood of encountering human hosts. ii Acknowledgments I would like to acknowledge my supervisor, Dr. Cyril Guyard, for his continuous tutelage in both matters academic and non-academic, without his direction I would not be the scientist I am today. I would also like to thank Dr. Mauricio Terebiznik, Dr. Alex Ensminger and Dr. Roberto Melano for their continuous support and guidance over the course of my scientific training. They have been instrumental to my learning process, and I am indebted to the help they have given me. In addition, I would like to thank Carla Duncan and Dr. Mohammed Adil Khan for their valuable advice throughout my training. iii Table of Contents Abstract........................................................................................................................................................ ii Acknowledgments ..................................................................................................................................... iii List of Figures ............................................................................................................................................ vi List of Appendices................................................................................................................................... viii Chapter 1: Introduction ................................................................................................................................1 1.1 Legionella pneumophila and legionellosis. .....................................................................................1 1.2 Protozoa and L. pneumophila biofilm formation............................................................................4 1.3 Attachment and Physiochemical Determinants of L. pneumophila Biofilm Formation and Colonization. .........................................................................................................................................6 1.4 Regulation of L. pneumophila Biofilm Formation ...........................................................................8 1.5 The Role of Non‐Protozoa Microbial Species in L. pneumophila Biofilm Colonization.................11 1.6 The Resistance of L. pneumophila Containing Biofilms to Biocides..............................................12 1.7 Auto‐aggregation and Biofilm Production. ...................................................................................16 1.8 The Role of Lcl in L. pneumophila Adhesion and Virulence ..........................................................16 1.9 The study.......................................................................................................................................18 Chapter 2: The role of Lcl in L. pneumophila auto‐aggregation and host‐phagocyte interactions ............19 2.1 Introduction ..................................................................................................................................19 2.2 Materials and Methods.................................................................................................................20 2.3 Results...........................................................................................................................................27 2.4 Discussion......................................................................................................................................55 Chapter 3: The Role of Lcl Collagenous Repeats in L. pneumophila Biofilm Production, Attachment and Adhesion. ....................................................................................................................................................59 3.1 Introduction ..................................................................................................................................59 3.2 Materials and Methods.................................................................................................................61 3.3 Results...........................................................................................................................................69 3.4 Discussion......................................................................................................................................89 4 Conclusion................................................................................................................................................93 References ..................................................................................................................................................94 iv List of Tables Table 1. L. pneumophila Strains used in Chapter 2. Table 2. Table 2. Non-L. pneumophila strains used in Chapter 2. Table 3. The PCR primers used in Chapter 2. Table 4. L. pneumophila strains used in Chapter 3. Table 5. PCR primers used in Chapter 3. Table 6. Comparison of predicted amino acid sequences in Lcl isoforms. v List of Figures Figure 1. Monospecies biofilm of the L. pneumophila lab strain Lp02 stained with the membrane permeable DNA dye Syto62. Figure 2. Acanthamoeba castellanii infected with Lp02 expressing green fluorescent protein (GFP). Figure 3. Schematic of the endogenous and environmental factors that influence L. pneumophila (Lp) biofilm production and colonization. Figure 4. L. pneumophila sediments more efficiently than Legionella non- pneumophila strains. Figure 5. Lcl is essential for L. pneumophila auto-aggregation. Figure 6. Divalent cations are required for Lcl dependent auto-aggregation. Figure 7. Surface exposed Lcl is required for L. pneumophila auto-aggregation. Figure 8. Lcl alone is sufficient to induce auto-aggregation and biofilm production Figure 9. Production of Lcl alters E. coli sediment ultrastructure. Figure 10. Lcl mediates the attachment of L. pneumophila to Acanthamoeba castellanii. Figure 11. Lcl dependent auto-aggregation potentiates the internalization of L. pneumophila in A. castellanii. Figure 12. Fucoidan inhibits L. pneumophila sedimentation in a dose dependent manner. Figure 13. Lcl dependent auto-aggregation increases the number of L. pneumophila per infected A. castellanii Figure 14. Polymorphisms in the number of lpg2644 collagenous repeats are positively correlated to biofilm production in clinical isolates. Figure 15. Clinical isolates LU1536, LR1063 and LR0347 contain size polymorphisms in their predicted Lcl sequences. Figure 16. Schematic representation of the different Lcl isoforms in this study. Figure 17. The number of Lcl collagenous repeats are correlated with L. pneumophila biofilm production in an isogenic background. Figure 18. Lcl collagenous repeats impact L. pneumophila-abiotic surface interactions. vi Figure 19. Lcl collagenous repeats influence L. pneumophila cell-cell interactions and sedimentation. Figure 20. Lcl collagenous repeats mediate L. pneumophila biofilm structure. Figure 21. The number of Lcl collagenous repeats influences fucoidan binding of L. pneumophila and recombinant Lcl. Figure 22. Lcl collagenous repeats influence L. pneumophila clinical prevalence. Figure 23. Lcl influences L. pneumophila surface hydrophobicity. vii List of Appendices Abbreviations PFA (Paraformaldehyde) Mip (Macrophage infectivity potentiator) Hsp60 (Heat shock protein 60) GFP (Green Fluorescent protein) Lp (Legionella pneumophila) PBS (Phospate Buffered Saline) c-di-GMP (Cyclic Di-Guanosine Monophosphate) Lcl (Legionella collagen-like protein) IPTG (Isopropyl β-D-1-thiogalactopyranoside) CFU (Colony Forming Units) CLSM (Confocal Laser Scanning Microscopy) GAG (Glycosaminoglycan) BYE (Buffered Yeast Extract) BCYE (Buffered Charcoal Yeast Extract) ELISA (Enzyme Linked Immunosorbant Assay) OD (Optical Density) SDS-PAGE (Sodium Dodecyl Sulfate Polyacrylimade Gel Electrophoresis) BSA (Bovine Serum Albumen) WT (Wild-type) KO (Knock-out) PCR (Polymerase Chain Reaction) qPCR (Quantitative PCR) viii ECM (Extracellular Matrix) MOI (Multiplicity of Infection) TCA (Trichloroacetic Acid) LB (Luria
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