Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths

By Marie Touchon, C. Hoede, O. Tenaillon, V. Barbe, Simon Baeriswyl, P. Bidet, É. Bingen, S. Bonacorsi, C. Bouchier, O. Bouvet and 31 more. PLoS Genetics, 2009

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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.

Subfields: Endocrinology, Genetics, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/7759d1f562985b56c54e892d1ad3b834b138f48f

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Citations in the corpus

Environmental Escherichia coli: ecology and public health implications—a review (2017, background): “coli, including environmental strains, which is also of great concern for public health (Touchon et al. 2009; Wellington et al. 2013).”
Mobility of Plasmids (2010, background): “Although rampant recombination could have taken place and eroded phylogenetic lineages, this has not happened, because some core genes are rarely successfully exchanged (88, 141).”
Recent Advances in Understanding Enteric Pathogenic Escherichia coli (2013, background): “coli is therefore largely afforded by the flexible gene pool through the gain and loss of genetic material at a number of hot spots throughout the genome (23) (Fig.”
Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. (2011, background): “The problem is that the taxa recognized as species by bacterial systematics are extremely broadly defined, with enormous levels of divergence in physiology, genome content, and most importantly, ecology (Welch et al., 2002; Whittam & Bumbaugh, 2002; Tettelin et al., 2005; Lefébure & Stanhope, 2007; ”
Prospective Genomic Characterization of the German Enterohemorrhagic Escherichia coli O104:H4 Outbreak by Rapid Next Generation Sequencing Technology (2011, methodology): “The Ion Torrent reads were assembled using the publicly available EAEC 55989 genome sequence [11] in a referenceguided strategy.”
The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. (2013, background): “The second and more common reason is E. coli’s highly variable gene content that is driven by the frequent gain and loss of genes (Touchon et al., 2009).”
The Pangenome: Diversity, Dynamics and Evolution of Genomes (2020, background): “Moreover, despite gene flow, core-genomes have conserved the phylogenetic signal of the vertical inheritance of bacterial taxa (Touchon et al. 2009; Abby et al. 2012).”
Survival of Escherichia coli in the environment: fundamental and public health aspects (2011, background): “coli genomes is now better understood than ever before (Kudva et al., 2002; Touchon et al., 2009).”
Microbiology and the species problem (2010, background): “For examples where the recombination and phylogenetic approaches sort organisms into different species, see Touchon et al. (2009).”
The human gut microbiome: ecology and recent evolutionary changes. (2011, background): “coli strains; the total gene pool exceeded 10,000 genes (99).”
Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. (2011, background): “coli encompassing nearly 18 000 genes despite the fact that the coding content of a single cell of this species is slightly over 2000 genes (Touchon et al., 2009).”
The population genetics of commensal Escherichia coli (2010, background): “Hence, each strain or group of strains contains some genes sampled from a pool that currently contains up to 8,000 genes (excluding insertion sequences, phage and phage-like elements, as well as core genes) but that keeps increasing with the number of strains studie”
Molecular mechanisms of Escherichia coli pathogenicity (2012, background): “coli isolates are thought to have a core genome of approximately 2,200 genes and a pan-genome of approximately 13,000 gene”