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1. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths.

Author

Marie Touchon, Claire Hoede, Olivier Tenaillon, Valérie Barbe, Simon Baeriswyl, Philippe Bidet, Edouard Bingen, Stéphane Bonacorsi, Christiane Bouchier, Odile Bouvet, Alexandra Calteau, Hélène Chiapello, Olivier Clermont, Stéphane Cruveiller, Antoine Danchin, Médéric Diard, Carole Dossat, Meriem El Karoui, Eric Frapy, Louis Garry, Jean Marc Ghigo, Anne Marie Gilles, James Johnson, Chantal Le Bouguénec, Mathilde Lescat, Sophie Mangenot, Vanessa Martinez-Jéhanne, Ivan Matic, Xavier Nassif, Sophie Oztas, Marie Agnès Petit, Christophe Pichon, Zoé Rouy, Claude Saint Ruf, Dominique Schneider, Jérôme Tourret, Benoit Vacherie, David Vallenet, Claudine Médigue, Eduardo P C Rocha, and Erick Denamur

Subjects
Genetics, QH426-470
Abstract

The Escherichia coli species represents one of the best-studied model organisms, but also encompasses a variety of commensal and pathogenic strains that diversify by high rates of genetic change. We uniformly (re-) annotated the genomes of 20 commensal and pathogenic E. coli strains and one strain of E. fergusonii (the closest E. coli related species), including seven that we sequenced to completion. Within the approximately 18,000 families of orthologous genes, we found approximately 2,000 common to all strains. Although recombination rates are much higher than mutation rates, we show, both theoretically and using phylogenetic inference, that this does not obscure the phylogenetic signal, which places the B2 phylogenetic group and one group D strain at the basal position. Based on this phylogeny, we inferred past evolutionary events of gain and loss of genes, identifying functional classes under opposite selection pressures. We found an important adaptive role for metabolism diversification within group B2 and Shigella strains, but identified few or no extraintestinal virulence-specific genes, which could render difficult the development of a vaccine against extraintestinal infections. Genome flux in E. coli is confined to a small number of conserved positions in the chromosome, which most often are not associated with integrases or tRNA genes. Core genes flanking some of these regions show higher rates of recombination, suggesting that a gene, once acquired by a strain, spreads within the species by homologous recombination at the flanking genes. Finally, the genome's long-scale structure of recombination indicates lower recombination rates, but not higher mutation rates, at the terminus of replication. The ensuing effect of background selection and biased gene conversion may thus explain why this region is A+T-rich and shows high sequence divergence but low sequence polymorphism. Overall, despite a very high gene flow, genes co-exist in an organised genome.

Published
2009
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2. Role of the vpe carbohydrate permease in Escherichia coli urovirulence and fitness in vivo

Author

Laurence du Merle, Chantal Le Bouguénec, Vanessa Martinez-Jéhanne, Christophe Pichon, Olivier Poupel, Christiane Bouchier, and Nadège Cayet

Subjects
Carbohydrate transport, Operon, Immunology, Mutant, Molecular Sequence Data, Virulence, Biology, Urine, medicine.disease_cause, Microbiology, Mice, medicine, Animals, Humans, Uropathogenic Escherichia coli, Phosphoenolpyruvate Sugar Phosphotransferase System, Escherichia coli, Genetics, Bacteriological Techniques, Permease, Escherichia coli Proteins, Wild type, Membrane Transport Proteins, Gene Expression Regulation, Bacterial, Molecular Pathogenesis, Complementation, Intestines, Infectious Diseases, Fermentation, Urinary Tract Infections, Mice, Inbred CBA, Carbohydrate Metabolism, Parasitology, Female, Gene Deletion
Abstract

Uropathogenic Escherichia coli (UPEC) strains are a leading cause of infections in humans, but the mechanisms governing host colonization by this bacterium remain poorly understood. Previous studies have identified numerous gene clusters encoding proteins involved in sugar transport, in pathogen-specific islands. We investigated the role in fitness and virulence of the vpe operon encoding an EII complex of the phosphotransferase (PTS) system, which is found more frequently in human strains from infected urine and blood (45%) than in E. coli isolated from healthy humans (15%). We studied the role of this locus in vivo , using the UPEC E. coli strain AL511, mutants, and complemented derivatives in two experimental mouse models of infection. Mutant strains displayed attenuated virulence in a mouse model of sepsis. A role in kidney colonization was also demonstrated by coinfection experiments in a mouse model of pyelonephritis. Electron microscopy examinations showed that the vpeBC mutant produced much smaller amounts of a capsule-like surface material than the wild type, particularly when growing in human urine. Complementation of the vpeBC mutation led to an increase in the amount of exopolysaccharide, resistance to serum killing, and virulence. It was therefore clear that the loss of vpe genes was responsible for all the observed phenotypes. We also demonstrated the involvement of the vpe locus in gut colonization in the streptomycin-treated mouse model of intestinal colonization. These findings confirm that carbohydrate transport and metabolism underlie the ability of UPEC strains to colonize the host intestine and to infect various host sites.

Published
2012

3. Role of deoxyribose catabolism in colonization of the murine intestine by pathogenic escherichia coli strains

Author

Maria Damian, Arnaud Fontanet, Codruta Usein, Malika Gouali, Chantal Le Bouguénec, Vanessa Martinez-Jéhanne, Christine Bernier-Fébreau, Amy Gassama-Sow, Laurence du Merle, Yves Germani, Bernadette Coddeville, Awa Aïdara-Kane, Yann Guérardel, Abdul-Aziz Wane, Pathogénie Bactérienne des Muqueuses, Institut Pasteur [Paris], Molecular Epidemiology Laboratory, Cantacuzino Institute [Romania], Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP), Institut Pasteur de Dakar, Réseau International des Instituts Pasteur (RIIP), Institut Pasteur de Bangui, Unité de Bactériologie Expérimentale, World Health Organisation (WHO), Organisation Mondiale de la Santé / World Health Organization Office (OMS / WHO), Epidémiologie des Maladies Emergentes - Emerging Diseases Epidemiology, Pasteur-Cnam Risques infectieux et émergents (PACRI), Institut Pasteur [Paris]-Conservatoire National des Arts et Métiers [CNAM] (CNAM)-Institut Pasteur [Paris]-Conservatoire National des Arts et Métiers [CNAM] (CNAM), Unité de Glycobiologie Structurale et Fonctionnelle UMR 8576 (UGSF), Institut National de la Recherche Agronomique (INRA)-Université de Lille-Centre National de la Recherche Scientifique (CNRS), Institut Pasteur de Madagascar, Pathogénie Microbienne Moléculaire, Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Epidémiologie des Maladies Emergentes, Pasteur-Cnam risques infectieux et émergents (PACRI), Unité de Glycobiologie Structurale et Fonctionnelle - UMR 8576 (UGSF), Université de Lille-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), Institut Pasteur [Paris] (IP), Institut Pasteur [Paris] (IP)-Conservatoire National des Arts et Métiers [CNAM] (CNAM), HESAM Université - Communauté d'universités et d'établissements Hautes écoles Sorbonne Arts et métiers université (HESAM)-HESAM Université - Communauté d'universités et d'établissements Hautes écoles Sorbonne Arts et métiers université (HESAM)-Institut Pasteur [Paris] (IP)-Conservatoire National des Arts et Métiers [CNAM] (CNAM), HESAM Université - Communauté d'universités et d'établissements Hautes écoles Sorbonne Arts et métiers université (HESAM)-HESAM Université - Communauté d'universités et d'établissements Hautes écoles Sorbonne Arts et métiers université (HESAM), and Université de Lille-Centre National de la Recherche Scientifique (CNRS)

Subjects
Adult, Diarrhea, Adolescent, Immunology, Colony Count, Microbial, Virulence, medicine.disease_cause, Microbiology, 03 medical and health sciences, chemistry.chemical_compound, Mice, Young Adult, Pathogenic Escherichia coli, Ribose, Operon, medicine, Escherichia coli, Animals, Humans, Colonization, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], Escherichia coli Infections, 030304 developmental biology, 0303 health sciences, biology, 030306 microbiology, Deoxyribose, Escherichia coli Proteins, Bacterial Infections, biology.organism_classification, Enterobacteriaceae, 3. Good health, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biomolecules [q-bio.BM], Intestines, Infectious Diseases, chemistry, Host-Pathogen Interactions, Parasitology, Bacteria
Abstract

We previously suggested that the ability to metabolize deoxyribose, a phenotype encoded by the deoK operon, is associated with the pathogenic potential of Escherichia coli strains. Carbohydrate metabolism is thought to provide the nutritional support required for E. coli to colonize the intestine. We therefore investigated the role of deoxyribose catabolism in the colonization of the gut, which acts as a reservoir, by pathogenic E. coli strains. Molecular and biochemical characterization of 1,221 E. coli clones from various collections showed this biochemical trait to be common in the E. coli species (33.6%). However, multivariate analysis evidenced a higher prevalence of sugar-metabolizing E. coli clones in the stools of patients from countries in which intestinal diseases are endemic. Diarrhea processes frequently involve the destruction of intestinal epithelia, so it is plausible that such clones may be positively selected for in intestines containing abundant DNA, and consequently deoxyribose. Statistical analysis also indicated that symptomatic clinical disorders and the presence of virulence factors specific to extraintestinal pathogenic E. coli were significantly associated with an increased risk of biological samples and clones testing positive for deoxyribose. Using the streptomycin-treated-mouse model of intestinal colonization, we demonstrated the involvement of the deoK operon in gut colonization by two pathogenic isolates (one enteroaggregative and one uropathogenic strain). These results, indicating that deoxyribose availability promotes pathogenic E. coli growth during host colonization, suggest that the acquisition of this trait may be an evolutionary step enabling these pathogens to colonize and persist in the mammalian intestine.

Published
2009
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4. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths

Author

Edouard Bingen, Olivier Clermont, Chantal Le Bouguénec, Zoé Rouy, Sophie Oztas, James R. Johnson, Anne-Marie Gilles, Erick Denamur, Marie Touchon, Olivier Tenaillon, David Vallenet, Valérie Barbe, Marie-Agnès Petit, Meriem El Karoui, Stéphane Bonacorsi, Dominique Schneider, Louis Garry, Eduardo P. C. Rocha, Alexandra Calteau, Antoine Danchin, Xavier Nassif, Ivan Matic, Vanessa Martinez-Jéhanne, Jérôme Tourret, Sophie Mangenot, Christophe Pichon, Jean Marc Ghigo, Claude Saint Ruf, Philippe Bidet, Claire Hoede, Eric Frapy, Christiane Bouchier, Simon Baeriswyl, Benoit Vacherie, Stéphane Cruveiller, Mathilde Lescat, Odile Bouvet, Carole Dossat, Claudine Médigue, Médéric Diard, Hélène Chiapello, Atelier de BioInformatique (ABI), Université Pierre et Marie Curie - Paris 6 (UPMC), Génomique évolutive des microbes, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Ecologie et Evolution des Microorganismes (EEM), Université Paris 13 (UP13)-Université Paris Diderot - Paris 7 (UPD7)-Université Sorbonne Paris Cité (USPC)-Institut National de la Santé et de la Recherche Médicale (INSERM), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Génétique moléculaire, évolutive et médicale, IFR65-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 7, Hôpital Robert Debré-Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM), Génomique (Plate-Forme) - Genomics Platform, Institut Pasteur [Paris] (IP), Génomique métabolique (UMR 8030), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Mathématique, Informatique, et Génomique, Institut National de la Recherche Agronomique (INRA), Génétique des Génomes Bactériens, Pathogénie des infections systémiques (UMR_S 570), Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Génétique des Biofilms, Veterans Affairs Medical Center, Department of Medecine, University of Minnesota [Twin Cities] (UMN), University of Minnesota System-University of Minnesota System, Pathogénie Bactérienne des Muqueuses, Unité des Bactéries Lactiques et Pathogènes Opportunistes, Laboratoire Adaptation et pathogénie des micro-organismes [Grenoble] (LAPM), Université Joseph Fourier - Grenoble 1 (UJF)-Centre National de la Recherche Scientifique (CNRS), Gagnon, Jean, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot - Paris 7 (UPD7)-Université Paris 13 (UP13)-Université Sorbonne Paris Cité (USPC)-Institut National de la Santé et de la Recherche Médicale (INSERM), Génomique (Plate-Forme), Institut Pasteur [Paris], University of Minnesota [Twin Cities], IFR65-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], Centre National de la Recherche Scientifique (CNRS)-Université Joseph Fourier - Grenoble 1 (UJF), Atelier de BioInformatique ( ABI ), Université Pierre et Marie Curie - Paris 6 ( UPMC ), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique ( CNRS ), Ecologie et Evolution des Microorganismes ( EEM ), Université Paris 13 ( UP13 ) -Université Paris Diderot - Paris 7 ( UPD7 ) -Université Sorbonne Paris Cité ( USPC ) -Institut National de la Santé et de la Recherche Médicale ( INSERM ), Genoscope - Centre national de séquençage [Evry] ( GENOSCOPE ), Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ), IFR65-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 ), Hôpital Robert Debré-Université Paris Diderot - Paris 7 ( UPD7 ) -Institut National de la Santé et de la Recherche Médicale ( INSERM ), Génomique métabolique ( UMR 8030 ), Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université d'Évry-Val-d'Essonne ( UEVE ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ), Institut National de la Recherche Agronomique ( INRA ), Pathogénie des infections systémiques ( UMR_S 570 ), Université Paris Descartes - Paris 5 ( UPD5 ) -Institut National de la Santé et de la Recherche Médicale ( INSERM ) -Centre National de la Recherche Scientifique ( CNRS ), University of Minnesota [Minneapolis], Laboratoire Adaptation et pathogénie des micro-organismes [Grenoble] ( LAPM ), and Université Joseph Fourier - Grenoble 1 ( UJF ) -Centre National de la Recherche Scientifique ( CNRS )

Subjects
MESH : Escherichia coli, Cancer Research, MESH : Polymorphism, Genetic, MESH : Recombination, Genetic, MESH : Models, Genetic, MESH : Models, Biological, MESH: Genome, Bacterial, Genome, MESH: Genetics, Gene flow, MESH : Genetics, MESH: Models, Genetic, MESH: Phylogeny, bioinformatique, Phylogeny, Genetics (clinical), MESH: Evolution, Molecular, Recombination, Genetic, bactérie, 2. Zero hunger, Genetics, Likelihood Functions, 0303 health sciences, Phylogenetic tree, MESH: Escherichia coli, MESH: Genomics, Genomics, Genome project, Evolutionary Biology/Microbial Evolution and Genomics, MESH: DNA Transposable Elements, MESH : DNA Transposable Elements, MESH: Recombination, Genetic, escherichia coli, MESH : Likelihood Functions, Research Article, lcsh:QH426-470, MESH : Genome, Bacterial, Biology, Models, Biological, Evolution, Molecular, 03 medical and health sciences, Phylogenetics, MESH: Polymorphism, Genetic, Escherichia coli, [SDV.BBM] Life Sciences [q-bio]/Biochemistry, Molecular Biology, MESH: Genome, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, MESH : Evolution, Molecular, Gene conversion, [ SDV.BBM ] Life Sciences [q-bio]/Biochemistry, Molecular Biology, Molecular Biology, Gene, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, Comparative genomics, Polymorphism, Genetic, Evolutionary Biology/Evolutionary and Comparative Genetics, Models, Genetic, 030306 microbiology, génome, MESH : Genomics, MESH: Models, Biological, MESH : Phylogeny, Microbiology/Medical Microbiology, lcsh:Genetics, DNA Transposable Elements, MESH: Likelihood Functions, MESH : Genome, Genome, Bacterial
Abstract

The Escherichia coli species represents one of the best-studied model organisms, but also encompasses a variety of commensal and pathogenic strains that diversify by high rates of genetic change. We uniformly (re-) annotated the genomes of 20 commensal and pathogenic E. coli strains and one strain of E. fergusonii (the closest E. coli related species), including seven that we sequenced to completion. Within the ∼18,000 families of orthologous genes, we found ∼2,000 common to all strains. Although recombination rates are much higher than mutation rates, we show, both theoretically and using phylogenetic inference, that this does not obscure the phylogenetic signal, which places the B2 phylogenetic group and one group D strain at the basal position. Based on this phylogeny, we inferred past evolutionary events of gain and loss of genes, identifying functional classes under opposite selection pressures. We found an important adaptive role for metabolism diversification within group B2 and Shigella strains, but identified few or no extraintestinal virulence-specific genes, which could render difficult the development of a vaccine against extraintestinal infections. Genome flux in E. coli is confined to a small number of conserved positions in the chromosome, which most often are not associated with integrases or tRNA genes. Core genes flanking some of these regions show higher rates of recombination, suggesting that a gene, once acquired by a strain, spreads within the species by homologous recombination at the flanking genes. Finally, the genome's long-scale structure of recombination indicates lower recombination rates, but not higher mutation rates, at the terminus of replication. The ensuing effect of background selection and biased gene conversion may thus explain why this region is A+T-rich and shows high sequence divergence but low sequence polymorphism. Overall, despite a very high gene flow, genes co-exist in an organised genome., Author Summary Although abundant knowledge has been accumulated regarding the E. coli laboratory strain K-12, little is known about the evolutionary trajectories that have driven the high diversity observed among natural isolates of the species, which encompass both commensal and highly virulent intestinal and extraintestinal pathogenic strains. We have annotated or re-annotated the genomes of 20 commensal and pathogenic E. coli strains and one strain of E. fergusonii (the closest E. coli related species), including seven that we sequenced to completion. Although recombination rates are much higher than mutation rates, we were able to reconstruct a robust phylogeny based on the ∼2,000 genes common to all strains. Based on this phylogeny, we established the evolutionary scenario of gains and losses of thousands of specific genes, identifying functional classes under opposite selection pressures. This genome flux is confined to very few positions in the chromosome, which are the same for every genome. Notably, we identified few or no extraintestinal virulence-specific genes. We also defined a long-scale structure of recombination in the genome with lower recombination rates at the terminus of replication. These findings demonstrate that, despite a very high gene flow, genes can co-exist in an organised genome.

Published
2009
Full Text
View/download PDF

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