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Horizontal Transfer, Selection and Maintenance of Antibiotic Resistance Determinants

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Horizontal Transfer, Selection and Maintenance of Antibiotic Resistance Determinants Faculty of Health Sciences Department of Pharmacy Horizontal transfer, selection and maintenance of antibiotic resistance determinants Julia Kloos A dissertation for the degree of Philosophiae Doctor - March 2021 Horizontal transfer, selection and maintenance of antibiotic resistance determinants Julia Kloos A dissertation for the degree of Philosophiae Doctor March 2021 Microbial Pharmacology and Population Biology Research Group Department of Pharmacy Faculty of Health Sciences UiT The Arctic University of Norway Acknowledgements The presented work was carried out in the Microbial Pharmacology and Population Biology Research Group at the Department of Pharmacy (IFA), UiT The Arctic University of Norway. I am grateful to former and current colleagues and students at IFA that made me feel welcome ever since I started working here and made these last years so enjoyable. I would like to thank the Norwegian PhD School of Pharmacy and the National Graduate School in Infection Biology and Antimicrobials for providing travel grants and organizing meetings, which allowed me to explore the microbial world internationally. Most of all, I am deeply grateful to my main supervisor Pål Johnsen, for being full of enthusiasm, great ideas and good humor. I admire the way you share your profound knowledge and scientific experience with your students and colleagues and are available for questions, discussions and new results at any time. Your guidance and trust were always encouraging and invaluable to me - thank you! My co-supervisor Klaus Harms taught me many tips and tricks in microbiological laboratory methods since the first day I arrived at IFA, which encouraged me to consider a PhD in microbiology. Thank you, Klaus, for pondering with me on the many molecular puzzles that bacteria provide, patiently and enduringly. Thank you Ørjan for bringing smelly, interesting bugs to our lab, for your structured thinking, and fast and thorough feedback based on your great expertise in clinical microbiology. Finishing this PhD was only possible with the good colleagues I had. Thank you all for making MicroPop the diverse, lively and supportive research group that it is. To Ane, Elizabeth, Nicole, Conny and Iren: thank you for sharing both joy and frustration about lab life with me, and for all the trust and support. You are great scientific role models and friends to me. Thank you João, a.k.a. ‘team piggy’ co-responsible and ‘husband’, for allowing all the questions and discussions, and for being such a reliable companion. Dear Theresa, thank you for being my constant source of encouragement and inspiration. Our trips across northern Norway, exploring mountains on long tracks, mean a lot to me. Thank you Anke and Marita, for keeping our friendship alive over long distance and many years and being curious about my Tromsø-life and work. Thank you, Tony, for so much joy and support J. Danke and meine Familie ♡ Tromsø, March 2021 Julia Kloos Table of contents List of papers ..................................................................................................................................... II Abbreviations .................................................................................................................................. III Summary .......................................................................................................................................... IV Introduction ....................................................................................................................................... 1 Evolution of antibiotic resistance .................................................................................................... 1 Horizontal gene transfer ................................................................................................................ 13 Mobile genetic elements ................................................................................................................ 17 Bacterial fitness and cost of antibiotic resistance .......................................................................... 25 Reversibility of resistance ............................................................................................................. 33 Objectives ......................................................................................................................................... 38 Materials and Methods ................................................................................................................... 39 Bacterial species ............................................................................................................................ 39 Methodological approaches ........................................................................................................... 43 Summary of Results ......................................................................................................................... 48 Paper I: Conserved collateral antibiotic susceptibility networks in diverse clinical strains of Escherichia coli. ........................................................................................................................ 48 Paper II: Tn1-transposition in the course of natural transformation enables horizontal antibiotic resistance spread in Acinetobacter baylyi. ..................................................................................... 49 Paper III: Piggybacking on niche-adaptation improves the maintenance of multidrug resistance plasmids. ........................................................................................................................................ 50 Discussion ......................................................................................................................................... 51 Conclusion ........................................................................................................................................ 60 References ......................................................................................................................................... 61 I List of papers Paper I Podnecky, N.L., Fredheim, E.G.A., Kloos, J., Sørum, V., Primicerio, R., Roberts, A.P., Rozen, D.E., Samuelsen, Ø., Johnsen, P.J. Conserved collateral antibiotic susceptibility networks in diverse clinical strains of Escherichia coli. Nature Communications, 2018. https://doi.org/10.1038/s41467-018-06143-y Reprinted under the Creative Commons Attribution 4.0 International License Paper II Kloos, J., Johnsen, P.J., Harms, K. Tn1-transposition in the course of natural transformation enables horizontal antibiotic resistance spread in Acinetobacter baylyi. Microbiology, 2020. https://doi.org/10.1099/mic.0.001003 Reprinted under the Creative Commons Attribution 4.0 International License Paper III Kloos, J.*, Gama, J.A.*, Hegstad, J., Samuelsen, Ø., Johnsen, P.J. Piggybacking on niche-adaptation improves the maintenance of multidrug resistance plasmids. accepted manuscript Molecular Biology and Evolution, 2021 https://doi.org/10.1093/molbev/msab091 Reprinted under the Creative Commons Attribution 4.0 International License * These authors contributed equally to this work. II Abbreviations ArcAB Aerobic Respiration Control AST Antimicrobial Susceptibility Testing BMD Broth Microdilution CCR Carbon Catabolite Repression CR Collateral Resistance CS Collateral Sensitivity DHFR Dihydrofolate Reductase DR Direct Repeat dsDNA double-stranded DNA ESBL Extended Spectrum Beta-Lactamase EUCAST European Committee on Antimicrobial Susceptibility Testing G-/G+ Gram-negative/Gram-positive HGT Horizontal Gene Transfer IC90 Inhibitory Concentration 90% ICE Integrative Conjugative Element IR Inverted Repeat IS Insertion Sequence MDR Multidrug Resistance MGE Mobile Genetic Element MIC Minimal Inhibitory Concentration MPC Mutant Prevention Concentration MSC Minimal Selective Concentration MSW Mutant Selection Window NDM New-Delhi Metallo-β-lactamase PBP Penicillin-Binding Protein ssDNA single-stranded DNA ST Sequence Type TSD Target Site Duplication UPEC Uropathogenic E. coli UTI Urinary Tract Infection VIM Verona-Integron Metallo-β-lactamase WGS Whole Genome Sequencing III Summary The rapid emergence of antibiotic resistance in bacterial pathogens represents a substantial clinical and financial burden to our society. The development of antibiotics is generally unprofitable and challenged by the need for innovative and evolution-robust drugs. It is thus insufficient to rely on the discovery of new therapeutic agents, but important to understand the selection, spread and maintenance of bacterial antibiotic resistance in order to counteract its emergence. The work presented in this thesis focused on mechanisms and evolutionary dynamics underlying these factors. Collateral sensitivity, when bacterial resistance to one antibiotic potentiates the effect of other antibiotics, may be exploited in infection treatment to limit resistance evolution. We assessed collateral susceptibility changes in ten diverse isolates of single-drug resistant uropathogenic Escherichia coli towards 16 antibiotics and found conserved changes especially in ciprofloxacin resistant mutants. Collateral responses changed also another parameter important for resistance selection, the mutant prevention concentration, accordingly. We reveal that knowledge of the mechanism as well as the fitness cost of resistance supports the predictability of bacterial collateral responses in antibiotic resistant mutants (paper I).
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