The genetic basis of Escherichia coli pathoadaptation to macrophages.
Antagonistic interactions are likely important driving forces of the evolutionary process underlying bacterial genome complexity and diversity. We hypothesized that the ability of evolved bacteria to escape specific components of host innate immunity, such as phagocytosis and killing by macrophages...
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doaj-2f9e1ddc011c4aca9168fd2c0497aac72021-04-21T17:41:35ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742013-01-01912e100380210.1371/journal.ppat.1003802The genetic basis of Escherichia coli pathoadaptation to macrophages.Migla MiskinyteAna SousaAna SousaAna SousaRicardo S RamiroJorge A Moura de SousaJerzy KotlinowskiIris CaramalhoSara MagalhãesMiguel P SoaresIsabel GordoAntagonistic interactions are likely important driving forces of the evolutionary process underlying bacterial genome complexity and diversity. We hypothesized that the ability of evolved bacteria to escape specific components of host innate immunity, such as phagocytosis and killing by macrophages (MΦ), is a critical trait relevant in the acquisition of bacterial virulence. Here, we used a combination of experimental evolution, phenotypic characterization, genome sequencing and mathematical modeling to address how fast, and through how many adaptive steps, a commensal Escherichia coli (E. coli) acquire this virulence trait. We show that when maintained in vitro under the selective pressure of host MΦ commensal E. coli can evolve, in less than 500 generations, virulent clones that escape phagocytosis and MΦ killing in vitro, while increasing their pathogenicity in vivo, as assessed in mice. This pathoadaptive process is driven by a mechanism involving the insertion of a single transposable element into the promoter region of the E. coli yrfF gene. Moreover, transposition of the IS186 element into the promoter of Lon gene, encoding an ATP-dependent serine protease, is likely to accelerate this pathoadaptive process. Competition between clones carrying distinct beneficial mutations dominates the dynamics of the pathoadaptive process, as suggested from a mathematical model, which reproduces the observed experimental dynamics of E. coli evolution towards virulence. In conclusion, we reveal a molecular mechanism explaining how a specific component of host innate immunity can modulate microbial evolution towards pathogenicity.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24348252/?tool=EBI |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Migla Miskinyte Ana Sousa Ana Sousa Ana Sousa Ricardo S Ramiro Jorge A Moura de Sousa Jerzy Kotlinowski Iris Caramalho Sara Magalhães Miguel P Soares Isabel Gordo |
spellingShingle |
Migla Miskinyte Ana Sousa Ana Sousa Ana Sousa Ricardo S Ramiro Jorge A Moura de Sousa Jerzy Kotlinowski Iris Caramalho Sara Magalhães Miguel P Soares Isabel Gordo The genetic basis of Escherichia coli pathoadaptation to macrophages. PLoS Pathogens |
author_facet |
Migla Miskinyte Ana Sousa Ana Sousa Ana Sousa Ricardo S Ramiro Jorge A Moura de Sousa Jerzy Kotlinowski Iris Caramalho Sara Magalhães Miguel P Soares Isabel Gordo |
author_sort |
Migla Miskinyte |
title |
The genetic basis of Escherichia coli pathoadaptation to macrophages. |
title_short |
The genetic basis of Escherichia coli pathoadaptation to macrophages. |
title_full |
The genetic basis of Escherichia coli pathoadaptation to macrophages. |
title_fullStr |
The genetic basis of Escherichia coli pathoadaptation to macrophages. |
title_full_unstemmed |
The genetic basis of Escherichia coli pathoadaptation to macrophages. |
title_sort |
genetic basis of escherichia coli pathoadaptation to macrophages. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS Pathogens |
issn |
1553-7366 1553-7374 |
publishDate |
2013-01-01 |
description |
Antagonistic interactions are likely important driving forces of the evolutionary process underlying bacterial genome complexity and diversity. We hypothesized that the ability of evolved bacteria to escape specific components of host innate immunity, such as phagocytosis and killing by macrophages (MΦ), is a critical trait relevant in the acquisition of bacterial virulence. Here, we used a combination of experimental evolution, phenotypic characterization, genome sequencing and mathematical modeling to address how fast, and through how many adaptive steps, a commensal Escherichia coli (E. coli) acquire this virulence trait. We show that when maintained in vitro under the selective pressure of host MΦ commensal E. coli can evolve, in less than 500 generations, virulent clones that escape phagocytosis and MΦ killing in vitro, while increasing their pathogenicity in vivo, as assessed in mice. This pathoadaptive process is driven by a mechanism involving the insertion of a single transposable element into the promoter region of the E. coli yrfF gene. Moreover, transposition of the IS186 element into the promoter of Lon gene, encoding an ATP-dependent serine protease, is likely to accelerate this pathoadaptive process. Competition between clones carrying distinct beneficial mutations dominates the dynamics of the pathoadaptive process, as suggested from a mathematical model, which reproduces the observed experimental dynamics of E. coli evolution towards virulence. In conclusion, we reveal a molecular mechanism explaining how a specific component of host innate immunity can modulate microbial evolution towards pathogenicity. |
url |
https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24348252/?tool=EBI |
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