The decoupling between genetic structure and metabolic phenotypes in <i>Escherichia coli</i> leads to continuous phenotypic diversity

Sabarly, Victor; Bouvet, Odile; Glodt, Jérémy; Clermont, Olivier; Skurnik, David; Diancourt, Laure; Vienne, Dominique de; Denamur, Erick; Dillmann, Christine

doi:10.1111/j.1420-9101.2011.02287.x

Cited by 36 publications

(35 citation statements)

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“…Moreover, it has been reported that the survival of E. coli is also greatly influenced by previous exposure to stress (19). Thus, beyond the variance related to the design of experiments, the obtained results also illustrate the extensive genetic and phenotypic diversity exhibited within E. coli populations, which could explain the different survival abilities in aquatic environments (3,8,23,24).…”

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confidence: 73%

“…Because E. coli populations have extensive genetic and phenotypic diversities (3,8,23,24), we tried to explain these different survival abilities by studying the genotypic and phenotypic traits involved in strain persistence in aquatic environments. The presence of an E. coli genotype related to persistent and naturalized strains was already described in temperate and tropical freshwater conditions (15,17,26,42).…”

Section: Discussionmentioning

confidence: 99%

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Evidence for Coexistence of Distinct Escherichia coli Populations in Various Aquatic Environments and Their Survival in Estuary Water

Berthe

Ratajczak

Clermont

et al. 2013

Appl Environ Microbiol

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b Escherichia coli, a commensal bacterium from the intestinal tracts of humans and vertebrate animals, has been used as one of two bacterial indicators of fecal contamination, along with intestinal enterococci, to monitor the microbiological quality of water. However, water environments are now recognized as a secondary habitat where some strains can survive. We investigated the survival of E. coli isolates collected from bodies of water in France exhibiting distinct profiles of contamination, defined according to the following criteria: vicinity of the point sources of contamination, land use, hydrology, and physicochemical characteristics of the receiving water. We selected 88 E. coli strains among a collection of 352 strains to carry out a microcosm experiment in filtered estuarine water for 14 days at 10°C. The relationship between the survival of E. coli strains and genotypic and phenotypic characteristics was analyzed. This work showed that distinct E. coli survival types, able to survive from between 7 and 14 days to less than 2 days, coexisted in the water. E. coli isolates that rapidly lost their culturability were more frequently isolated in water recently contaminated by fecal bacteria of human origin, and most were multiresistant to antibiotics and harbored several virulence factors. In contrast, persistent strains able to survive from 4 to 14 days were more often found in water with low levels of fecal bacteria, belonged mainly to the B1 phylogroup, often harbored only one virulence factor, kspE or ompT, and were able to grow at 7°C.

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confidence: 73%

Section: Discussionmentioning

confidence: 99%

Evidence for Coexistence of Distinct Escherichia coli Populations in Various Aquatic Environments and Their Survival in Estuary Water

Berthe

Ratajczak

Clermont

et al. 2013

Appl Environ Microbiol

Self Cite

124

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“…Such intraspecies diversity of the growth rate in different media (40,41) and of the RpoS level (42,43) has been reported in other sets of E. coli strains, with no link to the commensal or pathogenic origin of the strains concerned being found. Studies of growth yield on 95 carbon sources in 168 Escherichia strains also demonstrated a high level of diversity that was not structured into groups but that was continuous, with the lifestyle of the strains having almost no impact on growth yield (44). Natural isolates of E. coli have been shown to display various endogenous oxidative stresses when grown in urine, regardless of their origin or pathogenic potential (37).…”

Section: Discussionmentioning

confidence: 99%

Fitness, Stress Resistance, and Extraintestinal Virulence in Escherichia coli

et al. 2013

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eThe extraintestinal virulence of Escherichia coli is dependent on numerous virulence genes. However, there is growing evidence for a role of the metabolic properties and stress responses of strains in pathogenesis. We assessed the respective roles of these factors in strain virulence by developing phenotypic assays for measuring in vitro individual and competitive fitness and the general stress response, which we applied to 82 commensal and extraintestinal pathogenic E. coli strains previously tested in a mouse model of sepsis. Individual fitness properties, in terms of maximum growth rates in various media (Luria-Bertani broth with and without iron chelator, minimal medium supplemented with gluconate, and human urine) and competitive fitness properties, estimated as the mean relative growth rate per generation in mixed cultures with a reference fluorescent E. coli strain, were highly diverse between strains. The activity of the main general stress response regulator, RpoS, as determined by iodine staining of the colonies, H 2 O 2 resistance, and rpoS sequencing, was also highly variable. No correlation between strain fitness and stress resistance and virulence in the mouse model was found, except that the maximum growth rate in urine was higher for virulent strains. Multivariate analysis showed that the number of virulence factors was the only independent factor explaining the virulence in mice. At the species level, growth capacity and stress resistance are heterogeneous properties that do not contribute significantly to the intrinsic virulence of the strains.

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“…Bacterial metabolism is arguably the most promising model system for such an endeavour: the ability to metabolize different nutrient sources always remains an essential determinant of bacterial fitness 2 , and flux balance analysis (FBA) has been established as a robust and reliable modeling framework for the prediction of this ability 7 . Experimental growth data indicates that genetic distance, based on multilocus sequence typing data, is a weak indicator of how similar two E. coli strains are in terms of the carbon sources they can metabolize 1 . Similarly, a computational analysis of automatically generated metabolic models for hundreds of species suggested that withinspecies phenotypic divergence is almost instantaneous, while divergence between genera is gradual or "clock-like" 2 .…”

Section: Introductionmentioning

confidence: 99%

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AbstractEven closely related prokaryotes show an astounding diversity in their ability to grow in different nutritional environments 1,2 ; more fundamentally, it is unknown what fraction of metabolic adaptations are indeed complex. Here, we use metabolic network simulations to show that all 3,363 phenotypic innovations observed in the evolutionary history of 53 E. coli strains arose through the acquisition of a single DNA segment; while we found no evidence for the contribution of selectively neutral processes, 10.6% of adaptations to previously unviable environments relied on the support of DNA acquisitions on earlier phylogenetic branches.

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The adaptive acquisition of single DNA segments drives metabolic evolution acrossE. colilineages

Pang

Lercher

2017

Preprint

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Even closely related prokaryotes show an astounding diversity in their ability to grow in different nutritional environments 1,2 ; more fundamentally, it is unknown what fraction of metabolic adaptations are indeed complex. Here, we use metabolic network simulations to show that all 3,363 phenotypic innovations observed in the evolutionary history of 53 E. coli strains arose through the acquisition of a single DNA segment; while we found no evidence for the contribution of selectively neutral processes, 10.6% of adaptations to previously unviable environments relied on the support of DNA acquisitions on earlier phylogenetic branches. 97.0% of all metabolic phenotypes accessible for the E. coli pan-genome could be bestowed on any ancestral strain by transferring a single DNA segment from one of the extant strains. These results demonstrate an amazing ability of the E. coli lineage to quickly adapt to previously inaccessible environments through a single DNA acquisition, an ability likely to be mirrored in other clades of generalist bacteria.

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The decoupling between genetic structure and metabolic phenotypes in Escherichia coli leads to continuous phenotypic diversity

Cited by 36 publications

References 75 publications

Evidence for Coexistence of Distinct Escherichia coli Populations in Various Aquatic Environments and Their Survival in Estuary Water

Evidence for Coexistence of Distinct Escherichia coli Populations in Various Aquatic Environments and Their Survival in Estuary Water

Fitness, Stress Resistance, and Extraintestinal Virulence in Escherichia coli

The adaptive acquisition of single DNA segments drives metabolic evolution acrossE. colilineages

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