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Evolutionary Genomics of Conjugative Elements and Integrons

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Evolutionary Genomics of Conjugative Elements and Integrons Université Paris Descartes École doctorale Interdisciplinaire Européenne 474 Frontières du Vivant Microbial Evolutionary Genomic, Pasteur Institute Evolutionary genomics of conjugative elements and integrons Thèse de doctorat en Biologie Interdisciplinaire Présentée par Jean Cury Pour obtenir le grade de Docteur de l’Université Paris Descartes Sous la direction de Eduardo Rocha Soutenue publiquement le 17 Novembre 2017, devant un jury composé de: Claudine MÉDIGUE Rapporteure CNRS, Genoscope, Évry Marie-Cécile PLOY Rapporteure Université de Limoges Érick DENAMUR Examinateur Université Paris Diderot, Paris Philippe LOPEZ Examinateur Université Pierre et Marie Curie, Paris Alan GROSSMAN Examinateur MIT, Cambdridge, USA Eduardo ROCHA Directeur de thèse CNRS, Institut Pasteur, Paris ِ عمحمود ُبدرويش َالنرد َم ْن انا ِٔ َقول ُلك ْم ما ا ُقول ُلك ْم ؟ وانا لم أ ُك ْن َ َج ًرا َص َق َل ْت ُه ُالمياه َفأ ْص َب َح ِوهاً و َق َصباً َثق َب ْت ُه ُالرياح َفأ ْص َب َح ًنايا ... انا ِع ُب َالن ْرد ، ا َرب ُح يناً وا َس ُر يناً انا ِم ُثل ُك ْم ا وا قل قليً ... The dice player Mahmoud Darwish Who am I to say to you what I am saying to you? I was not a stone polished by water and became a face nor was I a cane punctured by the wind and became a lute… I am a dice player, Sometimes I win and sometimes I lose I am like you or slightly less… Contents Acknowledgments 7 Preamble 9 I Introduction 11 1 Background for friends and family . 13 2 Horizontal Gene Transfer (HGT) . 16 2.1 Mechanisms of horizontal gene transfer . 16 2.1.1 Transformation . 16 2.1.2 Conjugation . 17 2.1.3 Transduction . 18 2.1.4 Other mechanisms . 18 2.2 Evolutionary consequences . 20 2.2.1 HGT and bacterial ecology . 20 2.2.2 HGT and bacterial chromosome . 21 3 Mobile Genetic Elements (MGE) . 25 3.1 Different types of MGE . 25 3.2 Persistence of MGE . 27 3.2.1 Replication . 28 3.2.2 Partition system . 29 3.2.3 Integration . 34 4 Deciphering the bacterial chromosome . 36 4.1 Formal grammars . 37 4.2 Hidden Markov Model profiles . 38 4.3 Covariance Models . 40 5 II Contributions 43 1 Conjugation 45 1.1 Introduction . 45 1.1.1 Background . 45 1.1.2 Diversity . 46 1.1.3 Mechanism . 47 1.1.4 Objectives . 49 1.2 Methods . 51 1.2.1 Article 1: Identifying conjugative plasmids and integrative conjugative elements with CONJScan . 51 1.3 Results . 79 1.3.1 Article 2: Integrative and conjugative elements and their hosts: com- position, distribution, and organization . 79 1.3.2 Article 3: Host range expansion and genetic plasticity drive the trade-off between integrative and extra-chromosomal mobile genetic elements . 94 1.4 Conclusion . 125 2 Integrons 129 2.1 Introduction . 129 2.1.1 Background . 129 2.1.2 Diversity . 129 2.1.3 Mechanism . 130 2.1.4 Objectives . 132 2.2 Methods and Results . 133 2.2.1 Article 4: Identification and analysis of integrons and cassettes arrays in bacterial genomes . 133 2.2.2 Article 5: Differences in Integron Cassette Excision Dynamics Shape a Trade-Off between Evolvability and Genetic Capacitance . 146 2.3 Conclusion . 163 III Conclusions and Perspectives 167 Bibliography 179 Annexes 195 6 Remerciements Je voudrais d’abord remercier Eduardo de m’avoir proposé de faire une thèse dans son labo, alors que je comptais encore faire des manips à l’époque! Ça fera quasiment trois quatre cinq ans passés dans ton labo, et je dois dire que ce fût un réel plaisir d’y travailler (et pas seulement grâce à la terrasse!). Toute cette thèse ne serait pas grand chose sans ton encadrement, ta disponibilité, ton savoir encyclopédique, et ta confiance. Un grand merci aussi à Marie de m’avoir guidé dans les arcanes de la bioinfoEduardique. Cette thèse n’aurait pas été un tel plaisir sans ce bureau 07E. Il est d’abord très bien placé, au 6ème étage d’un bâtiment neuf, il offre un accès direct à une terrasse plein sud de plus de 100m2, tout en étant suffisamment distant du bureau du boss, permettant une arrivée en douce à toute heure de la journée. Ce bureau ne serait rien sans les 3 co-thésardes qui m’ont accompagné dans ce périple et sans qui d’inestimables discussions n’auraient jamais eu lieu, au grand dam du monde probablement. Camille, Aude, Camille, merci d’avoir supporté mes bruits, mon bordel, mes pulls troués, mes plantes, la doc. Vous m’avez fait aussi perdre vachement de temps. Merci pour tout. Je voudrais aussi remercier tous ces gens que j’ai vu défiler dans ce labo, qui ont aussi participé à sa richesse, et qui d’une façon ou d’une autre ont participé à ce travail. Merci à Brigitte pour toute sa disponibilité. Tout cette aventure est devenue possible grâce à la rencontre de deux personnes clés qui m’ont conduit à pousser la porte du labo d’Eduardo. D’abord Julian qui m’a initié à la mi- crobiologie en toute simplicité, en me montrant quels solvants pouvait être pipetés à la bouche pour étudier un truc1 trouvé en forêt. Julian m’a encouragé à aller travailler avec Didier, grâce à qui j’ai pu continuer mon apprentissage de la microbiologie, entouré d’une équipe décapante. Merci pour tout Didier, désolé pour les librairies, mais merci de m’avoir conseillé d’aller faire ce stage chez Eduardo. Un grand merci aux Marsouins et à ce groupe de compères aimant la recherche comme la Chouffe, mainenant dispersés à travers le monde: Jehanne, Antoine, Aleks, Antoine, Clément, Ariane, Paul, Aude, Vincent, Fati, Hassen, Khalifa, les frites. Merci au CRI et à ce qu’il est et à tous les gens géniaux qu’on peut y croiser. Beaucoup ont déjà été cités précédemment. Je rajouterai juste Flora, merci d’avoir partagé ton énergie en tant que représentante des étudiants, 1un “slime mold”, après enquête 7 ou en tant que co-organisatrice (avec Aleks) des Visionary & Retrospective talks. La thèse m’a rendu un peu plus solitaire que je ne le suis déjà, mais merci à tous les potos d’être là, en Albanie, à Marseille, à Essernay, à Alrance, sur l’ile d’Houat, ou à Pernes. Théo, merci pour ce subtil soutien depuis bien longtemps. Nono, JibJib, NicNic merci de m’avoir laissé vous conduire à Mont de Marsan en Che Clio Sudaka. Julie merci d’avoir lancé ma carrière d’acteur. Gregoire Chéron. Merci à mon ami Meidi pour ces nombreuses années à se charier. Merci à Marjo pour la soupe aux courgettes. Ma photo officielle sur le site de l’Institut Pasteur — un jour d’été, en revenant de Bora-Bora — vous est naturellement dédié, Léo, Charlie, Antoine, Édith, Alexis, John, avec qui j’ai fait mes premiers bacs et mes premiers rappels sur arbre mort. Merci à mes parents et ma sœur pour leur soutien et encouragements. Merci à Didine d’être la meilleure grand-mère. Merci au reste de la famille pour les discussions passionées à toute heure et à rosé. Merci à Jehanne pour tout ce que tu m’apportes depuis 9 ans, 5 mois et 1 jour. C’est inédit. Merci aux correcteurs de cette thèse, ma mère, Aleks et Jehanne. 8 Preamble The goal of this thesis is to develop and evaluate methods to study two types of genetic elements whose role in the spread of antibiotic resistance genes is no longer to be demonstrated. Conjugative elements on the one hand are known for their ability to spread among a wide range of bacteria and their plasticity allows them to carry numerous functions, and notably antibiotic resistance genes. On the other hand, integrons are known for their specific capacity to capture genes and rearrange them to minimize the fitness cost for the bacteria. They have been particularly successful in capturing antibiotic resistance genes. Research carried on these elements has been mainly focused on variants carrying antibiotic resistance genes, highly successful in pathogenic bacteria. However, the broader evolutionary picture of these elements remains sparse as efficient tools to detect them in bacterial genomes are lacking. In Part I, I introduce the key concepts of horizontal gene transfer and mobile genetic el- ements as they play a major role in bacterial evolution. Conjugative elements and integrons are two different types of mobile genetic elements, and they spread in bacterial populations through horizontal gene transfer. I also present the basics of two methods on which the tools and methods developed in this thesis are heavily relying on. Part II will present the contributions I made regarding these two elements. In chapter 1, I present a method that allows the detection of conjugative elements and the delimitation of integrative and conjugative elements at large scale, without imposing an a priori on the functions carried by the elements. In chapter 2, I present a tool that identifies integrons in bacterial genomes, not restricted to previously discovered integrons. Both methods allowed to produce the largest and most genetically diverse datasets of the corresponding elements so far. Each chapter also presents the subsequent analysis made on these datasets. Together, this work aims at better understanding these elements, with the goal of providing tools and knowledge to improve their surveillance. It also sheds light on the evolution of mobile genetic elements in general, and fuels, at its scale, the global understanding of bacterial evolution. 9 10 Part I Introduction 11 Introduction 1 Background for friends and family The Resistance Awakens. Bacteria represent one of the three kingdoms of life, together with Archaea and Eucaryotes.
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