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Thèses Traditionnelles UNIVERSITÉ D’AIX-MARSEILLE FACULTÉ DE MÉDECINE DE MARSEILLE ECOLE DOCTORALE DES SCIENCES DE LA VIE ET DE LA SANTÉ THÈSE Présentée et publiquement soutenue devant LA FACULTÉ DE MÉDECINE DE MARSEILLE Le 23 Novembre 2017 Par El Hadji SECK Étude de la diversité des procaryotes halophiles du tube digestif par approche de culture Pour obtenir le grade de DOCTORAT d’AIX-MARSEILLE UNIVERSITÉ Spécialité : Pathologie Humaine Membres du Jury de la Thèse : Mr le Professeur Jean-Christophe Lagier Président du jury Mr le Professeur Antoine Andremont Rapporteur Mr le Professeur Raymond Ruimy Rapporteur Mr le Professeur Didier Raoult Directeur de thèse Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR 7278 Directeur : Pr. Didier Raoult 1 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 3 Sommaire AVANT PROPOS 3 RESUME / ABSTRACT 6/8 INTRODUCTION 9 CHAPITRE I : Répertoire des prokaryotes halophiles isolés chez l’homme (revue). 13 Article 1: Halophilic and halotolerant prokaryotes in Human. 17 Soumis dans Future Microbiology CHAPITRE II : Étude de la diversité des prokaryotes halophiles du tube digestif par 55 culturomics et effet du sel sur la variation du microbiome halophile. 59 Article 2: Salinity and the Neglected Human Gut Halophilic Microbiome. Soumis dans Nature Article 3: Culture of previously uncultured members of the human gut microbiota by 83 culturomics. Publié dans Nature Microbiology CHAPITRE III : Évaluation de la survie des pathogènes de l’Homme dans l’eau de mer. 93 Article 4: Very low risk of bacterial infection in sea water. 97 Soumis dans Lancet Infectious Diseases CHAPITRE IV : Descriptions des nouvelles espèces halophiles isolées par taxonogenomics 117 Article 5: Virgibacillus senegalensis sp. nov. a moderately halophilic bacterium 123 isolated from the human gut. Publié dans New Microbes New Infections 135 Article 6: Non contiguous-finished genome sequence and description of Planococcus massiliensis sp. nov. a moderately halophilic bacterium isolated from the human gut. Publié dans New Microbes New Infections Article 7: Halomonas massiliensis’ sp. nov., a new halotolerant bacterium isolated from 147 the human gut. Publié dans New Microbes New Infections Article 8: Description of “Bacillus dakarensis sp. nov.”, “Bacillus sinesaloumensis sp. nov.”, “Gracilibacillus timonensis sp .nov”.,“Halobacillus massiliensis sp. nov.”, 149 “Lentibacillus massiliensis sp. nov.”, “Oceanobacillus senegalensis sp. nov.”, “Oceanobacillus timonensis sp. nov.”, “Virgibacillus dakarensis sp. nov.”, “Virgibacillus marseillensis sp. nov.”, nine halophilic new species isolated from human stool. Publié dans New Microbes New Infections 4 Article 9 enome sequence and description of Gracilibacillus timonensis sp. nov., a : G 157 moderate halophile isolate from gut. Soumis dans MicrobiologyOpen Article 10: Microbial culturomics to isolate halophilic bacteria from table salt: 191 Genome sequence and description of the moderately halophilic bacterium Bacillus salis sp. nov. Publié dans New Microbes New Infections Article 11: ‘Gracilibacillus phocaeensis’ sp. nov., ‘Sediminibacillus massiliensis’ sp. 211 nov. and ‘Virgibacillus ndiopensis’ sp. nov., three halophilic species isolated from salty human stools by culturomics. Accepté dans New Microbes New Infections CHAPITRE V : (ANNEXES) : Travaux collaboratifs sur la description de nouvelles espèces 225 isolées par culturomics. Article 12: Bacillus kwashiokori gen. nov., sp. nov., a new bacterial genus isolated from 231 a malnourished child using culturomics. Publié dans MicrobiologyOpen Article 13: Tessaracoccus massiliensis sp. nov., a new bacterial species isolated from 245 human gut. Publié dans New Microbes New Infections CONCLUSIONS ET PERSPECTIVES 255 REFERENCES 257 5 Résumé L'alimentation est le principal déterminant du microbiote intestinal. Ces dernières années beaucoup d'études se sont penchées sur son rôle dans la variation du microbiote intestinal. Cependant, la plupart des études qui lient le régime alimentaire et le microbiote intestinal sont axées sur les macronutriments comme les glucides, les graisses et les protéines, mais le rôle des micronutriments et des minéraux tel que le NaCl a été négligé à ce jour. Le sel est un minéral essentiel à la vie humaine et l'un des assaisonnements alimentaires les plus anciens et les plus omniprésents. Le salage est la méthode la plus ancienne de conservation des aliments. Cependant, une consommation élevée de sel a été associée à l'obésité, au syndrome métabolique, à l'hypertension artérielle, aux maladies cardiovasculaires, au cancer gastrique, aux maladies auto-immunes et à la mortalité toutes causes confondues. Plusieurs mécanismes sous-jacents, y compris le stress oxydatif, ont été étudiés. Mais la salinité dans l'intestin et l'altération possiblement associée de son microbiote, récemment identifiées comme un symbiote critique de la santé et de la maladie, n'ont pas encore été explorées chez l'homme. Ici, en testant 1334 prélèvements de selles, nous avons montré qu'une salinité élevée était associée à une diminution de la diversité globale et à l'émergence de populations microbiennes halophiles dans l'intestin. La salinité fécale était associée au régime alimentaire salé et à l'obésité, conformément aux données épidémiologiques. Aucun procaryote halophile n’a été cultivé en dessous d'un seuil de salinité fécale de 1,5 %. Au-delà de ce seuil, nous avons découvert une diversité inattendue de microbiote halophile humain dont la richesse était corrélée avec les concentrations de sel; 64 espèces différentes ont été isolées, dont 21 nouvelles espèces et 43 espèces connues dans l'environnement mais non chez les humains. Trois procaryotes extrêmement halophiles ont été isolés, dont deux Archaea appartenant au genre Haloferax, avec une nouvelle espèce Haloferax massiliensis, et un nouveau genre bactérien, Halophilibacterium massiliense. La découverte d'une telle diversité de procaryotes halophiles chez l'homme est assez surprenante. En effet, les procaryotes halophiles sont décrits comme des micro-organismes vivants dans des environnements hypersalés tels que l'eau de mer. La composition microbienne de l'eau de mer est principalement dominée par des bactéries halophiles. En effet plus de la moitié d'entre elles sont halophiles, qui ne sont qu’occasionnellement pathogènes pour l'homme. C'est l'une des raisons pour lesquelles, dans la littérature, il existe peu de preuves que les infections peuvent être contractées directement par l'eau de mer. Néanmoins, cela contraste avec le nombre de mesures de la qualité de l'eau organisées pour prévenir le risque d'infection humaine. Il nous a paru intéressant de vérifier au laboratoire si les bactéries pathogènes humaines étaient susceptibles de se développer dans l'eau de mer. En conclusion, nous avons démontré que la plupart des bactéries citées en microbiologie clinique n'ont pas survécu longtemps dans les eaux marines en raison de 6 nombreux facteurs, y compris la salinité. Les maladies marines sont dominées par les infections à Vibrio et Shewenalla. Nous avons estimé que les dépenses considérables consacrées à la prévention des infections marines ne sont pas fondées sur des données probantes. D'autres études sont nécessaires pour réévaluer le risque infectieux associé à l’eau de mer afin de réadapter les politiques de surveillance des eaux marines. Mots-clés : microbiote digestif, halophile, sel, NaCl, eau de mer, infection, pathogène. 7 Abstract Diet is the main determinant of gut microbiota. In recent years many studies have looked at its role in the variation of the gut microbiota. However, most studies linking diet and gut microbiota focus on macronutrients such as carbohydrates, fats and proteins, but the role of micronutrients and minerals such as NaCl have been neglected to date. Salt is an essential mineral to human life and one of the oldest and the most ubiquitous dietary seasoning, and salting is an important and oldest method of preserving food. However, elevated salt consumption has been associated with obesity, metabolic syndrome, high blood pressure, cardiovascular disease, gastric cancer, autoimmune disease and all- cause mortality. Several underlying mechanisms, including oxidative stress, have been investigated, but salinity in human gut and the possible associated alteration of its microbiota recently identified as a critical symbiote of health and disease, have not yet
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