Trade-off between bile resistance and nutritional competence drives Escherichia coli diversification in the mouse gut
| Autor: | Nadine Cerf-Bensussan, Dominique Rainteau, François Taddei, Sabine Rakotobe, Marianne De Paepe, Valérie Gaboriau-Routhiau |
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| Přispěvatelé: | Interactions de l'épithelium intestinal et du système immunitaire (UMR_S 793), Institut National de la Recherche Agronomique (INRA)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), MICrobiologie de l'ALImentation au Service de la Santé (MICALIS), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Inflammation intestinale, Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Robustesse et évolvabilité de la vie (U1001), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris Descartes - Paris 5 (UPD5), MDP was supported by the Fondation pour la Recherche Médicale (http://www.frm.org/)., Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Recherche Agronomique (INRA), Interactions de l'épithelium intestinal et du système immunitaire ( UMR_S 793 ), Institut National de la Santé et de la Recherche Médicale ( INSERM ) -Université Paris Descartes - Paris 5 ( UPD5 ) -Institut National de la Recherche Agronomique ( INRA ), MICrobiologie de l'ALImentation au Service de la Santé humaine ( MICALIS ), Institut National de la Recherche Agronomique ( INRA ) -AgroParisTech, Université Pierre et Marie Curie - Paris 6 ( UPMC ) -Institut National de la Santé et de la Recherche Médicale ( INSERM ) -Centre National de la Recherche Scientifique ( CNRS ), Robustesse et évolvabilité de la vie ( U1001 ), Institut National de la Santé et de la Recherche Médicale ( INSERM ) -Université Paris Descartes - Paris 5 ( UPD5 ), Autard, Delphine |
| Jazyk: | angličtina |
| Rok vydání: | 2011 |
| Předmět: |
Operon
Mutant Genetic Fitness MESH: Escherichia coli Proteins Mice MESH : Selection Genetic MESH: Animals 0303 health sciences MESH : Trans-Activators MESH: Escherichia coli Escherichia coli Proteins Microbiology and Parasitology Bacterial SDV:GEN MESH: Transcription Factors MESH : Multienzyme Complexes Microbiologie et Parasitologie MESH : Phenotype [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology Animals Bacterial Outer Membrane Proteins Bile Acids and Salts Biodiversity DNA-Binding Proteins Escherichia coli Flagella Gastrointestinal Tract Gene Expression Regulation Immunity Innate Multienzyme Complexes Mutation Nutritional Physiological Phenomena Phenotype Selection Genetic Trans-Activators Transcription Factors MESH : DNA-Binding Proteins MESH : Gene Expression Regulation Bacterial MESH: Phenotype Microbiology MESH: Flagella MESH: Biodiversity 03 medical and health sciences Genetics [SDV.MP] Life Sciences [q-bio]/Microbiology and Parasitology Molecular Biology Biology Ecology Evolution Behavior and Systematics [SDV.GEN]Life Sciences [q-bio]/Genetics MESH : Genetic Fitness 030306 microbiology MESH: Bacterial Outer Membrane Proteins Immunity Innate Colonisation Regulon MESH : Nutritional Physiological Phenomena MESH: Gastrointestinal Tract MESH : Gastrointestinal Tract [ SDV.GEN ] Life Sciences [q-bio]/Genetics Cancer Research MESH : Escherichia coli MESH : Transcription Factors MESH: Selection Genetic [SDV.GEN] Life Sciences [q-bio]/Genetics Gut flora medicine.disease_cause MESH: Multienzyme Complexes MESH: Genetic Fitness [ SDV.MP ] Life Sciences [q-bio]/Microbiology and Parasitology MESH : Biodiversity Genetics (clinical) 2. Zero hunger Experimental evolution MESH: Gene Expression Regulation Bacterial biology MESH : Escherichia coli Proteins MESH : Immunity Innate MESH: Immunity Innate MESH : Mutation Research Article MESH: Mutation lcsh:QH426-470 MESH: Trans-Activators MESH: Bile Acids and Salts Model Organisms MESH : Mice medicine Selection Genetic MESH: Nutritional Physiological Phenomena MESH : Bacterial Outer Membrane Proteins MESH: Mice 030304 developmental biology Evolutionary Biology Gene Expression Regulation Bacterial biology.organism_classification MESH : Bile Acids and Salts lcsh:Genetics bacteria MESH : Animals MESH : Flagella MESH: DNA-Binding Proteins |
| Zdroj: | PLoS Genetics PLoS Genetics, Public Library of Science, 2011, 7 (6), pp.e1002107. ⟨10.1371/journal.pgen.1002107⟩ PLoS Genetics, 2011, 7 (6), pp.e1002107. ⟨10.1371/journal.pgen.1002107⟩ PLoS Genetics, Public Library of Science, 2011, 7 (6), pp.e1002107. 〈10.1371/journal.pgen.1002107〉 PLoS Genetics, Vol 7, Iss 6, p e1002107 (2011) Plos Genetics 6 (7), e1002107. (2011) |
| ISSN: | 1553-7390 1553-7404 |
| DOI: | 10.1371/journal.pgen.1002107⟩ |
| Popis: | Bacterial diversification is often observed, but underlying mechanisms are difficult to disentangle and remain generally unknown. Moreover, controlled diversification experiments in ecologically relevant environments are lacking. We studied bacterial diversification in the mammalian gut, one of the most complex bacterial environments, where usually hundreds of species and thousands of bacterial strains stably coexist. Herein we show rapid genetic diversification of an Escherichia coli strain upon colonisation of previously germ-free mice. In addition to the previously described mutations in the EnvZ/OmpR operon, we describe the rapid and systematic selection of mutations in the flagellar flhDC operon and in malT, the transcriptional activator of the maltose regulon. Moreover, within each mouse, the three mutant types coexisted at different levels after one month of colonisation. By combining in vivo studies and determination of the fitness advantages of the selected mutations in controlled in vitro experiments, we provide evidence that the selective forces that drive E. coli diversification in the mouse gut are the presence of bile salts and competition for nutrients. Altogether our results indicate that a trade-off between stress resistance and nutritional competence generates sympatric diversification of the gut microbiota. These results illustrate how experimental evolution in natural environments enables identification of both the selective pressures that organisms face in their natural environment and the diversification mechanisms. Author Summary The mechanisms generating the huge biodiversity on earth are not entirely understood. Bacterial populations are powerful models to explore the mechanisms of evolution, owing to their big population size, rapid growth, and high mutation rate. One of the more complex bacterial community is the mammalian gut microbiota, and Escherichia coli is one of the first colonizers of the newborn intestine. Herein we studied diversification of an Escherichia coli strain in germ-free mice, a simplified though ecologically relevant system. We show rapid genetic diversification upon colonization, characterized by the systematic selection of mutations in three different pathways: in the global regulator EnvZ/OmpR controlling outer membrane permeability, in the flagellar operon, and in the maltose regulon. By combining in vivo and in vitro experiments, we show that the selective forces that drive E. coli diversification are the presence of bile salts and the competition for nutrients. Altogether our results indicate that a trade-off between stress resistance and nutritional competence is sufficient to mediate diversification of bacteria. These results illustrate how experimental evolution in natural environments allows the identification of the selective pressures that organisms face in their natural environment, as well as the diversification mechanisms. |
| Databáze: | OpenAIRE |
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