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

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 GarryJean 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, Erick Denamur

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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.

Original languageEnglish (US)
Article numbere1000344
JournalPLoS genetics
Issue number1
StatePublished - Jan 2009


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