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Michel ALHOSNY Les Maladies Associées À La Dysbiose

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Michel ALHOSNY Les Maladies Associées À La Dysbiose UNIVERSITÉ D’AIX-MARSEILLE FACULTÉ DE MÉDECINE T H È S E Soutenue publiquement le 22 Novembre 2018 En vue de l’obtention du titre : Docteur de l’Université d’Aix-Marseille Discipline : Sciences de la Vie et de la Santé Spécialité : Pathologie humaine - Maladies Infectieuses Michel ALHOSNY Les Maladies Associées à la Dysbiose Explorées par Analyse Génomique Composition du jury : Professeur F. FENOLLAR Université d’Aix-Marseille Président du jury Professeur J.P. LAVIGNE Université de Montpellier Rapporteur Professeur T.A. TRAN Université de Montpellier Rapporteur Professeur B. LA SCOLA Université d’Aix-Marseille Directeur de thèse Faculté de médecine, Aix-Marseille Université UM63, Institut de Recherche pour le Développement IRD 198, Assistance Publique – Hôpitaux de Marseille (AP-HM), Microbes, Evolution, Phylogeny and Infection (MEΦI), Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, Marseille, France. 1 2 Remerciements Je tiens à exprimer mes profondes remerciements à mon directeur de thèse Monsieur le Professeur Bernard La Scola, pour sa supervision au cours du déroulement de ce projet. Celui-ci n’aurait jamais été possible sans son soutien inconditionnel, ses conseils et ses qualités académiques remarquables, qui m’ont permis de surmonter les difficultés rencontrées au cours de la réalisation de ce travail. Vous n’étiez pas juste mon superviseur, mais un père pour moi ! Je remercie Monsieur le Professeur Didier Raoult de m’avoir accueilli au sein de l’Institut Hospitalo-Universitaire, Méditerranée-Infection ; un environnement scientifique particulier, stimulant l’esprit de recherche. Je remercie Madame le Professeur Florence Fenollar, d’avoir accepté de présider au sein du jury de cette Thèse. Je remercie messieurs les Professeurs Jean-Philippe Lavigne et Tu Anh Tran d’avoir accepté de siéger au sein du jury de cette Thèse et pour l’intérêt porté à ce travail. Je remercie mes parents; Sayed et Rima, mon frère Mario et ma petite sœur Leandra, pour leurs encouragements et leur soutien moral pendant ces trois années de séjour en France. C’est grâce à vous que je suis arrivé à ce stade. Merci, pour votre confiance et présence. Il me paraît important de remercier la plus belle rencontre de ma vie, signée par la présence de Rita Abou Abdallah et Jacques Bou Khalil, avec qui j’ai partagé beaucoup d’émotions et d’enthousiasmes. Le temps, l’attention, l’intérêt de votre disponibilité, m’avaient donné l’encouragement et la joie durant mon séjour à Marseille. Merci, pour votre confiance et support. J’ai partagé avec vous de moments inoubliables. On craint dégun, la famille ! Je remercie les services de l’Assistance Publique – Hôpitaux de Marseille (Hôpital de La Timone et La Conception), et des Centres Hospitaliers Universitaires (CHU Nîmes, CHU Nice et CHU Montpellier) pour la fourniture des prélèvements adéquats à notre projet de recherche. Je tiens à remercier mon équipe, également tous ceux qui ont contribué au succès de ce travail, en respectant leurs titres ; Jacques Bou Khalil, Anthony Levasseur, Philippe Colson, Nadim Cassir, Aurelia Caputo, Emeline Baptiste, Nathalie Wurtz, Muriel Militello, Clio Grimaldier, Nathalie Jaume, Lina Barrassi et Priscilla Jardot. Je remercie la Fondation Infectiopôle-Sud pour mon financement ainsi que pour le support financier de projets de recherche. J’adresse aussi les mots, et la place, ne suffiraient pas à exprimer toute ma reconnaissance envers tous ceux qui m’ont supporté et encouragé durant cette période. Merci à la famille Hosny et Féral de Dijon, mes tantes Sabah et Rose, mon oncle Ibrahim. En plus j’aimerais adresser mes remerciements à : Yolla Yaacoub, Rosalia Tannous, Joya Makhlouf, Marianne Samaha, Ranin Bechara, Jano et Théresa Fadlallah, Rana Melhem, Sergios Bou Francis. 3 4 Á Sayed, Rima, Mario et Leandra, aucune dédicace ne pourrait témoigner mon amour et mon affection envers vous. Rita et Jacques, toutes les lettres ne sauraient trouver les mots qu’il faut… Merci La mémoire de mon oncle le Dr. Michel Hosny, un rêve qui nous a quitté tôt, paix à son âme. Veuillez agréer mes respects les plus profondes et les affections les plus sincères. 5 6 Avant-propos Le format de présentation de cette thèse correspond à une recommandation de la spécialité Maladies Infectieuses et Microbiologie, à l’intérieur du Master des Sciences de la Vie et de la Santé qui dépend de l’Ecole Doctorale des Sciences de la Vie de Marseille. Le candidat est amené à respecter des règles qui lui sont imposées et qui comportent un format de thèse utilisé dans le Nord de l’Europe et qui permet un meilleur rangement que les thèses traditionnelles. Par ailleurs, la partie introduction et bibliographie est remplacée par une revue envoyée dans un journal afin de permettre une évaluation extérieure de la qualité de la revue et de permettre à l’étudiant de commencer le plus tôt possible une bibliographie exhaustive sur le domaine de cette thèse. Par ailleurs, la thèse est présentée sur article publié, accepté ou soumis associé d’un bref commentaire donnant le sens général du travail. Cette forme de présentation a paru plus en adéquation avec les exigences de la compétition internationale et permet de se concentrer sur des travaux qui bénéficieront d’une diffusion internationale. Professeur Didier RAOULT 7 8 Abstract Dysbiosis remains a main cause during the establishment of several diseases, by promoting pathogenic bacterial translocation, leading to the incorporation of inflammatory process within microbiota eco-system. Specific microorganisms were involved in the pathogenesis of dysbiosis-associated diseases, notably necrotizing enterocolitis (NEC) and diabetic foot (DF). From this, emerges the need to describe plausible relationship between diseases-associated microorganisms. This was possible by the implication of whole-genome analysis (WGA) approaches. Genomics analysis was combined with culture, targeted qPCR, genetic engineering and cytotoxicity to study the relationship between C. butyricum and the occurrence of NEC. A cohort was conducted in French South-East region, on matched preterm neonates stool samples and hospitalized in several neonatal intensive care unit (NICU). Culture showed that C. butyricum was the most frequently isolated species from NEC among Clostridia. By combining targeted culture and qPCR, we also showed a prevalence of C. butyricum significantly higher in NEC than controls. C. butyricum WGA revealed geographical and/or temporal clusters, thus genomic relationship between NEC- associated isolates and controls, suggesting the presence of asymptomatic carriage. Additionally, genes encoding for hemolysin were detected and C. butyricum supernatants from all clusters exhibited cytotoxic effect on Jurkat cells. Cytotoxic effect was also present on Caco-2 cell line, which directed the study towards the enteropathogenicity hypothesis. Supernatant of β-hemolysin-mutant C. butyricum showed enterotoxic effect. Based on physico-chemical data generated from fractioned supernatant, we assumed that the evaluated fraction was a protein, since enterotoxic activity was for the fractions greater than 30 KDa. Inactivation by heating-based tests confirmed our findings. FPLC and nano-LC-MS/MS performed on the same detected fraction revealed that PspC family transcriptional regulator was the unique cytotoxic protein identified. This protein owned a glucan-binding domain, 9 shared by C. difficile toxin A/B and S. pneumoniae autolysin. Genetic knock-out of PspC protein was cytotoxic on Caco-2 cells, suggesting by this the existence of different and/or the combination of encoding genes. In another study, we managed to explore the potential relationship between C. neonatale and NEC. Specific rpoB-based qPCR was developed to identify C. neonatale directly from patients’ samples. We found that, C. neonatale was more prevalent in NEC than in controls. Although co-identified in association with C. butyricum, C. neonatale showed lower abundance. In parallel, three geographic-related clonal lineage of C. neonatale were distinguished using WGA, especially in NEC-associated strains isolated from the same NICU. Hemolysin sequences were also identified. Furthermore, GNAT superfamily of acetyltransferase was the unique pathogenic family identified within two clusters, although not detected in the other cluster. These data suggest a mechanism similar to that of C. difficile infections, linked to antibiotics administration and toxin-producing species. Regarding to DF infection, single-nucleotide polymorphisms were used to study genomics evolution of S. aureus and E. coli, targeting the identification of mutations in coding regions, especially within virulent genes. Furthermore, taxonogenomics approach was used to characterize new bacterial species isolated from culturomics project. Finally, these results will highly contribute to the future studies and clinical application to decipher the occurrence of dysbiosis-linked diseases and their linkage to specific microorganism, in order to better understand its mechanism of physiopathology and targeted treatments. Keywords: Genomics, dysbiosis, necrotizing enterocolitis, Clostridium butyricum clonal lineage, enterotoxicity, Clostridium neonatale, diabetic feet, genetic evolution, taxonogenomics. 10 Résumé Au cours des dernières années, la dysbiose (ou déséquilibre de l'écosystème bactérien) a été identifiée comme une cause importante de survenues de maladies, favorisant la prolifération de bactéries pathogènes ou induisant des processus inflammatoires. L’étude de
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