MBE Advance Access published online on March 10, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh118
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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1 INSERM E0339, Faculté de Médecine Xavier Bichat, 16 rue Henri Huchard, 75018 Paris, France
* To whom correspondence should be addressed. E-mail: denamur{at}bichat.inserm.fr.
In bacteria, the evolution of pathogenicity seems to be the result of the constant arrival of virulence factors (VFs) into the bacterial genome. However, the integration, retention and/or expression of these factors may be the result of the interaction between the new arriving genes and the bacterial genomic background. To test this hypothesis, a phylogenetic analysis was done on a collection of 98 Escherichia coli/Shigella strains representing the pathogenic and commensal diversity of the species. The distribution of 17 VFs associated to the different E. coli pathovars was superimposed to the phylogenetic tree. Three major types of VFs can be recognized: (i) VFs that arrive and are expressed in different genetic backgrounds (like those associated to mild-chronic diarrhea's pathovars: enteroaggregative, enteropathogenic and diffusely-adhering E. coli), (ii) VFs that arrive in different genetic backgrounds but that are preferentially found, associated with a specific pathology, in only a particular background (like VFs associated to extraintestinal diseases) and, (iii) VFs that require a particular genetic background for the arrival and expression of their virulence potential (like those associated to pathovars typical of severe-acute diarrhea: enterohemorragic, enterotoxigenic and enteroinvasive E. coli strains). The possibility of a single arrival of VFs by chance, followed by a vertical transmission, is ruled out by comparing the evolutionary histories of some of these VFs to the strain phylogeny. These evidences suggest that important changes in the genome of E. coli have occurred during the diversification of the species allowing the virulence factors associated to severe-acute diarrhea to arrive in the population. Thus, the E. coli genome seems to be formed by an "ancestral" and a "derived" background, each one responsible for the acquisition and expression of different virulence factors. Key Words:
Escherichia coli, bacterial evolution, virulence, phylogeny
© 2004 Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved.
Original Articles
A Specific Genetic Background Is Required for Acquisition and Expression of Virulence Factors in Escherichia coli
2 UMR CNRS-IRD 9926, Centre IRD, 911 Avenue Agropolis, B.P. 64501, F-34394 Montpellier cedex 5, France
3 Centre d'Etude du Polymorphisme Humain, Hôpital Saint Louis, Paris, France
4 Unité de Pathogénie Bactérienne des Muqueuses, Institut Pasteur, Paris, France
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|
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|
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|
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|
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