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Bacterial Genomes, a Tale of Gene Transfer, Recombination and Cladogenesis Florent Lassalle

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Bacterial Genomes, a Tale of Gene Transfer, Recombination and Cladogenesis Florent Lassalle Bacterial genomes, a tale of gene transfer, recombination and cladogenesis Florent Lassalle To cite this version: Florent Lassalle. Bacterial genomes, a tale of gene transfer, recombination and cladogenesis. Pop- ulations and Evolution [q-bio.PE]. Université Claude Bernard - Lyon I, 2013. English. NNT : 2013LYO10234. tel-01214968 HAL Id: tel-01214968 https://tel.archives-ouvertes.fr/tel-01214968 Submitted on 13 Oct 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. No 234-2013 Année 2013 These` de l’universitede´ Lyon Présentée devant L’UNIVERSITÉ CLAUDE BERNARD LYON 1 pour l’obtention du Diplomeˆ de doctorat (arrêté du 7 août 2006) soutenue publiquement le 26 novembre 2013 par Florent Lassalle Les génomes bactériens, une histoire de transfert de gènes, de recombinaison et de cladogénèse. Directeurs de thèse : Xavier Nesme Vincent Daubin Jury : Céline Brochier-Armanet Examinateur Vincent Daubin Directeur de thèse Xavier Nesme Directeur de thèse Cécile Neuveglise´ Rapporteur Eduardo P. C. Rocha Examinateur J. Peter W. Young Rapporteur 2 UNIVERSITE CLAUDE BERNARD - LYON 1 Président de l’Université M. François-Noël GILLY Vice-président du Conseil d’Administration M. le Professeur Hamda BEN HADID Vice-président du Conseil des Etudes et de la Vie Univer- M. le Professeur Philippe LALLE sitaire Vice-président du Conseil Scientifique M. le Professeur Germain GILLET Directeur Général des Services M. Alain HELLEU COMPOSANTES SANTE Faculté de Médecine Lyon Est – Claude Bernard Directeur : M. le Professeur J. ETIENNE Faculté de Médecine et de Maïeutique Lyon Sud – Charles Directeur : Mme la Professeure C. BURILLON Mérieux Faculté d’Odontologie Directeur : M. le Professeur D. BOURGEOIS Institut des Sciences Pharmaceutiques et Biologiques Directeur : Mme la Professeure C. VIN- CIGUERRA Institut des Sciences et Techniques de la Réadaptation Directeur : M. le Professeur Y. MATILLON Département de formation et Centre de Recherche en Bi- Directeur : M. le Professeur P. FARGE ologie Humaine COMPOSANTES ET DEPARTEMENTS DE SCIENCES ET TECHNOLOGIE Faculté des Sciences et Technologies Directeur : M. le Professeur F. DE MARCHI Département Biologie Directeur : M. le Professeur F. FLEURY Département Chimie Biochimie Directeur : Mme le Professeur H. PARROT Département GEP Directeur : M. N. SIAUVE Département Informatique Directeur : M. le Professeur S. AKKOUCHE Département Mathématiques Directeur : M. le Professeur A. GOLDMAN Département Mécanique Directeur : M. le Professeur H. BEN HADID Département Physique Directeur : Mme S. FLECK Département Sciences de la Terre Directeur : Mme la Professeure I. DANIEL UFR Sciences et Techniques des Activités Physiques et Directeur : M. C. COLLIGNON Sportives Observatoire des Sciences de l’Univers de Lyon Directeur : M. B. GUIDERDONI Polytech Lyon Directeur : M. P. FOURNIER Ecole Supérieure de Chimie Physique Electronique Directeur : M. G. PIGNAULT Institut Universitaire de Technologie de Lyon 1 Directeur : M. C. VITON Institut Universitaire de Formation des Maîtres Directeur : M. A. MOUGNIOTTE Institut de Science Financière et d’Assurances Administrateur provisoire : M. N. LEBOISNE 4 Résumé Dans les génomes bactériens, les fréquents transferts horizontaux de gènes (HGT) intro- duisent des innovations génomiques qui peuvent entraîner la diversification des popula- tions bactériennes. À l’inverse, la recombinaison homologue (RH) au sein des populations homogénéise leurs génotypes, et ainsi renforce leur cohésion. Ces processus d’échange génétique, et la fréquence à laquelle ils interviennent au sein et entre les populations, doivent avoir un grand impact sur la cladogénèse bactérienne. Au-delà de la configuration des échanges qui se sont réellement produits entre les bactéries, les traces de RH et de HGT que nous observons dans leurs génomes reflètent les événements qui ont été fixés tout au long de leur histoire. Ce processus de fixation peut être biaisé en ce qui concerne la nature des gènes ou allèles qui ont été introduits. La sélection naturelle peut notamment conduire à la fixation des gènes transférés qui apportent de nouvelles adaptations écologiques. En outre, des biais mécaniques dans le processus de recombinaison lui-même peuvent con- duire à la fixation d’allèles non-adaptatifs. Nous avons cherché à caractériser certains de ces processus adaptatifs et non-adaptatifs qui façonnent les génomes bactériens. À cette fin, plusieurs aspects de l’évolution des génomes, comme les variations de leurs répertoires de gènes, de leur architecture et de leur composition en nucléotides ont été examinés à la lumière de leur histoire de transfert et de recombinaison. Les séquences génomiques des bactéries encodent la totalité de leurs adaptations écologiques et constituent en même temps l’enregistrement de l’histoire de leur diversification. Nous avons utilisé le complexe d’espèces Agrobacterium tumefaciens (At), un groupe divers de bactéries associées aux plantes comme modèle pour rechercher dans leurs génomes des sig- natures d’adaptations écologiques associées à leur histoire de diversification. Nous avons exploré la diversité du répertoire de gènes du taxon, d’abord en utilisant la technique d’hybridation génomique comparative (CGH), puis en utilisant les séquences génomiques pour reconstruire l’histoire évolutive des gènes dans les génomes. Pour ce faire, nous avons conçu une nouvelle approche phylogénétique pour la reconstruction de génomes ances- traux tenant compte des événements de transfert horizontal et de duplication des gènes. Cette approche identifie les groupes de gènes co-transférés ou co-dupliqués. L’utilisation de ce signal régional dans les génomes améliore la confiance et la précision de la datation des événements inférés. Les informations sur l’histoire reconstruite des génomes – y compris les arbres de gènes, les événements de transfert et de duplication, les blocs de gènes ayant co-évolué, les synténies, les annotations fonctionnelles ... – sont compilées dans une base de données intégrative, Agrogenom, et peuvent être visualisées et interrogées à travers une interface Web interactive. A partir des profils CGH et des génomes ancestraux reconstruits, nous avons identi- fié des gènes spécifiques des principaux clades au sein d’At. La plupart d’entre eux sont organisés en grands blocs de gènes ayant co-évolué et qui codent des voies métaboliques cohérentes. Cette organisation constitue une déviation par rapport à un modèle neutre de transfert, indiquant que ces gènes sont sous sélection purificatrice. Les gènes spécifiques de chaque espèce génomique et du complexe d’espèces At dans son ensemble codent de façon récurrente des fonctions liées à la production de métabolites secondaires sécrétés ou de matrice extra-cellulaire, ainsi que des fonctions référant au métabolisme de com- posés d’origine végétale tels que les composés phénoliques et les acides aminés. Ces gènes 5 spécifiques de clade définissent ainsi des micro-niches spécifiques au sein d’un même macro-environnement où l’interaction avec une plante hôte est primordiale. Ceci suggère que la différenciation écologique des clades d’At a eu lieu à travers le partitionnement des ressources écologiques disponibles dans la rhizosphère des plantes. D’après les histoires reconstituées des gènes, nous avons montré l’intensité des transferts de gènes au sein des espèces génomiques d’At, mais aussi l’occurrence de transferts entre espèces génomiques et clades plus anciens. Certains gènes définissant les niche écologiques ont parfois été partagés par des clades éloignés, ce qui a pu induire leur compétition pour des ressources partagées. Cependant, chaque clade est caractérisé par une combinaison spé- cifique de gènes prédisant des traits écologiques uniques, et dont l’expression semble être coordonnée par des systèmes de régulation impliquant la perception des signaux environ- nementaux spécifiques. Ce faisant, des clades divergents sont susceptibles de maintenir des niches écologiques différenciées, leur permettant de cohabiter dans l’habitat rhizosphérique. Une autre caractéristique des organismes cellulaires est le contenu en nucléotides G et C de leur génome, qui est connu pour varier considérablement entre génomes et en leur sein. Chez les mammifères, et probablement plus généralement chez les Eucaryotes, ces différences intra-génomiques du contenu en bases G et C (GC%) se révèlent être fortement influencées par les variations régionales dans les taux de recombinaison à long terme. Ceci est causé par un phénomène appelé conversion génique biaisée vers G/C (gBGC), qui favorise la fixation de mutations vers G ou C dans les régions de forte recombinaison. En revanche, au sein des génomes bactériens, l’hétérogénéité en GC% entre gènes est traditionnellement considérée comme une preuve de la multiplicité de leurs origines, en raison de transferts horizontaux fréquents, mais le mécanisme qui sous-tend la composition biaisée des gènes transférés est encore inconnu. Des études récentes ont suggéré qu’une mystérieuse force sélective favorisant un GC% plus élevé existe chez les bactéries, mais
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