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The population genetics of commensal Escherichia coli

Key Points

  • Escherichia coli is, paradoxically, both the most frequent commensal aero-anaerobic Gram-negative bacillus of the vertebrate gut and one of the main pathogens, being responsible for both intraintestinal and extraintestinal infections. Deciphering the ecological and evolutionary forces that shape the population structure of the commensal strains will help to understand the emergence of virulence in the species.

  • In the past few decades, successive molecular methods have contributed to the refinement of the clonal concept of E. coli, including serotyping and multilocus enzyme electrophoresis, followed by DNA marker analysis and nucleotide sequencing. Recently, whole-genome sequencing has revealed the organization of the genome and solved the contradiction between the occurence of recombination events and the observed clonality of the species, allowing the reconstruction of a robust phylogenetic history.

  • In parallel, population genetics-based epidemiology has shown that in a single individual there are predominant strains and also resident and transient strains. Clones, which are characterised by their phylogenetic group, are distributed according to environmental factors and the diet, gut morphology and body mass of their hosts.

  • Finally, the relationships between commensalism and virulence have been clarified. The coincidental hypothesis proposes that 'virulence factors' and their change in prevalence among hosts may reflect some local adaptation to commensal habitats rather than virulence per se. Likewise, intestinal microbiota has been shown to play an important part in the emergence of antibiotic resistance.

  • In the future, with the arrival of next-generation sequencing technology, the study of complete genomes of numerous isolates will allow the development of 'population genomics', and metagenomics approaches will take into account the vast accompanying intestinal microbiota that has been largely ignored in defining the commensal niche of E. coli.

Abstract

The primary habitat of Escherichia coli is the vertebrate gut, where it is the predominant aerobic organism, living in symbiosis with its host. Despite the occurrence of recombination events, the population structure is predominantly clonal, allowing the delineation of major phylogenetic groups. The genetic structure of commensal E. coli is shaped by multiple host and environmental factors, and the determinants involved in the virulence of the bacteria may in fact reflect adaptation to commensal habitats. A better characterization of the commensal niche is necessary to understand how a useful commensal can become a harmful pathogen. In this Review we describe the population structure of commensal E. coli, the factors involved in the spread of different strains, how the bacteria can adapt to different niches and how a commensal lifestyle can evolve into a pathogenic one.

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Figure 1: Escherichia coli core genome and pan-genome evolution according to the number of sequenced genomes.
Figure 2: Phylogenetic reconstruction and recombination.
Figure 3: Phylogenetic history of Escherichia coli.

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Acknowledgements

We are grateful to everyone who has helped us gather our strain collections over the years and continents and to all the members of our laboratory who have analysed these strains, especially P. Escobar-Páramo, T. Le Gall and O. Clermont. E.D. is partially funded by the Fondation pour la Recherche Médicale and O.T. is supported by the Agence Nationale de la Recherche. This review is dedicated to the memory of Thomas S. Whittam, a pioneer in E. coli population genetics, who died on 5 December 2008.

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Correspondence to Erick Denamur.

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DATABASES

Entrez Genome Project

Escherichia coli

Escherichia coli K-12

Escherichia fergusonii

Salmonella enterica

FURTHER INFORMATION

Authors' homepage

ECOR collection

MLST database at Michigan State University, USA

MLST database at Institut Pasteur Paris, France

MLST database at University College Cork, Ireland

Glossary

Panmictic

Pertaining to a population in which all individuals are potential recombination partners.

Overdominance

Occurs when natural selection favours the heterozygote over the homozygote in a diploid organism. Selectionists proposed overdominance as the driving force underlying the high level of polymorphism that is observed in natural populations.

Coalescent framework

Coalescent theory is a retrospective model of population genetics. It builds the genealogy of gene copies isolated from a sample of individuals from a population back to a single ancestral copy (known as the most recent common ancestor).

Approximate Bayesian computation

A family of computational likelihood-free inference techniques that operate on summary data (such as population mean or variance) to make broad inferences. They are especially useful in situations in which evaluation of the likelihood is computationally prohibitive or whenever suitable likelihoods are not available.

Linkage disequilibrium

The non-random association of alleles at two or more loci. It describes a situation in which some combinations of alleles or genetic markers occur more or less frequently in a population than would be expected if there were a random association of alleles on the basis of their frequencies.

MLEE-based phenogram

A dendrogram resulting from hierarchical clustering that is computed from multilocus enzyme electrophoresis (MLEE) data.

Long-branch attraction artefact

The erroneous grouping of two or more long branches as sister groups due to methodological artefacts of phylogenetic reconstruction. In the case discussed in this Review, a distant out-group (Salmonella enterica) works as an attractor of long-branched in-group taxa.

Colicin

A protein that is produced by and toxic for some strains of E. coli. Colicins result in the rapid elimination of neighbouring cells that are not resistant to their effects.

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Tenaillon, O., Skurnik, D., Picard, B. et al. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8, 207–217 (2010). https://doi.org/10.1038/nrmicro2298

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