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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Autores principales:	Migla Miskinyte, Ana Sousa, Ricardo S Ramiro, Jorge A Moura de Sousa, Jerzy Kotlinowski, Iris Caramalho, Sara Magalhães, Miguel P Soares, Isabel Gordo
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/2f9e1ddc011c4aca9168fd2c0497aac7
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spelling	oai:doaj.org-article:2f9e1ddc011c4aca9168fd2c0497aac72021-11-18T06:07:15ZThe genetic basis of Escherichia coli pathoadaptation to macrophages.1553-73661553-737410.1371/journal.ppat.1003802https://doaj.org/article/2f9e1ddc011c4aca9168fd2c0497aac72013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24348252/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Antagonistic 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.Migla MiskinyteAna SousaAna SousaAna SousaRicardo S RamiroJorge A Moura de SousaJerzy KotlinowskiIris CaramalhoSara MagalhãesMiguel P SoaresIsabel GordoPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 12, p e1003802 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 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.
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.
format	article
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
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)
publishDate	2013
url	https://doaj.org/article/2f9e1ddc011c4aca9168fd2c0497aac7
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The genetic basis of Escherichia coli pathoadaptation to macrophages.

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