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

ABSTRACT: To assess the extent of intra-species diversity and the links between phylogeny, lifestyle (habitat and pathogenicity) and phenotype, we assayed the growth yield on 95 carbon sources of 168 Escherichia strains. We also correlated the growth capacities of 14 E. coli strains with the presence/absence of enzyme-coding genes. Globally, we found that the genetic distance, based on multilocus sequence typing data, was a weak indicator of the metabolic phenotypic distance. Besides, lifestyle and phylogroup had almost no impact on the growth yield of non-Shigella E. coli strains. In these strains, the presence/absence of the metabolic pathways, which was linked to the phylogeny, explained most of the growth capacities. However, few discrepancies blurred the link between metabolic phenotypic distance and metabolic pathway distance. This study shows that a prokaryotic species structured into well-defined genetic and lifestyle groups can yet exhibit continuous phenotypic diversity, possibly caused by gene regulatory effects.

SUBMITTER: Sabarly V

PROVIDER: S-EPMC3147056 | biostudies-literature | 2011 Jul

REPOSITORIES: biostudies-literature

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

Sabarly V V Bouvet O O Glodt J J Clermont O O Skurnik D D Diancourt L L de Vienne D D Denamur E E Dillmann C C

Journal of evolutionary biology 20110513 7

To assess the extent of intra-species diversity and the links between phylogeny, lifestyle (habitat and pathogenicity) and phenotype, we assayed the growth yield on 95 carbon sources of 168 Escherichia strains. We also correlated the growth capacities of 14 E. coli strains with the presence/absence of enzyme-coding genes. Globally, we found that the genetic distance, based on multilocus sequence typing data, was a weak indicator of the metabolic phenotypic distance. Besides, lifestyle and phylog ...[more]

PMID: 21569155

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Project description:Although polymicrobial infections, caused by combinations of viruses, bacteria, fungi and parasites, are being recognised with increasing frequency, little is known about the occurrence of within-species diversity in bacterial infections and the molecular and evolutionary bases of this diversity. We used multiple approaches to study the genomic and phenotypic diversity among 226 Escherichia coli isolates from deep and closed visceral infections occurring in 19 patients. We observed genomic variability among isolates from the same site within 11 patients. This diversity was of two types, as patients were infected either by several distinct E. coli clones (4 patients) or by members of a single clone that exhibit micro-heterogeneity (11 patients); both types of diversity were present in 4 patients. A surprisingly wide continuum of antibiotic resistance, outer membrane permeability, growth rate, stress resistance, red dry and rough morphotype characteristics and virulence properties were present within the isolates of single clones in 8 of the 11 patients showing genomic micro-heterogeneity. Many of the observed phenotypic differences within clones affected the trade-off between self-preservation and nutritional competence (SPANC). We showed in 3 patients that this phenotypic variability was associated with distinct levels of RpoS in co-existing isolates. Genome mutational analysis and global proteomic comparisons in isolates from a patient revealed a star-like relationship of changes amongst clonally diverging isolates. A mathematical model demonstrated that multiple genotypes with distinct RpoS levels can co-exist as a result of the SPANC trade-off. In the cases involving infection by a single clone, we present several lines of evidence to suggest diversification during the infectious process rather than an infection by multiple isolates exhibiting a micro-heterogeneity. Our results suggest that bacteria are subject to trade-offs during an infectious process and that the observed diversity resembled results obtained in experimental evolution studies. Whatever the mechanisms leading to diversity, our results have strong medical implications in terms of the need for more extensive isolate testing before deciding on antibiotic therapies.

Project description:Filamentous phages are nonlytic viruses that specifically infect bacteria, establishing a persistent association with their host. The phage particle has no machinery for generating energy and parasitizes its host's existing structures in order to cross the bacterial envelope and deliver its genetic material. The import of filamentous phages across the bacterial periplasmic space requires some of the components of a macrocomplex of the envelope known as the Tol system. This complex uses the energy provided by the proton motive force (pmf) of the inner membrane to perform essential and highly energy-consuming functions of the cell, such as envelope integrity maintenance and cell division. It has been suggested that phages take advantage of pmf-driven conformational changes in the Tol system to transit across the periplasm. However, this hypothesis has not been formally tested. In order to decouple the role of the Tol system in cell physiology and during phage parasitism, we used mutations on conserved essential residues known for inactivating pmf-dependent functions of the Tol system. We identified impaired Tol complexes that remain fully efficient for filamentous phage uptake. We further demonstrate that the TolQ-TolR homologous motor ExbB-ExbD, normally operating with the TonB protein, is able to promote phage infection along with full-length TolA.IMPORTANCE Filamentous phages are widely distributed symbionts of Gram-negative bacteria, with some of them being linked to genome evolution and virulence of their host. However, the precise mechanism that permits their uptake across the cell envelope is poorly understood. The canonical phage model Fd requires the TolQRA protein complex in the host envelope, which is suspected to translocate protons across the inner membrane. In this study, we show that phage uptake proceeds in the presence of the assembled but nonfunctional TolQRA complex. Moreover, our results unravel an alternative route for phage import that relies on the ExbB-ExbD proteins. This work provides new insights into the fundamental mechanisms of phage infection and might be generalized to other filamentous phages responsible for pathogen emergence.

Dataset Information

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

Publications

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

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