Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131

ABSTRACT Escherichia coli ST131 is the most frequently isolated fluoroquinolone-resistant (FQR) E. coli clone worldwide and a major cause of urinary tract and bloodstream infections. Although originally identified through its association with the CTX-M-15 extended-spectrum β-lactamase resistance gen...

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Autores principales:	Nouri L. Ben Zakour, Areej S. Alsheikh-Hussain, Melinda M. Ashcroft, Nguyen Thi Khanh Nhu, Leah W. Roberts, Mitchell Stanton-Cook, Mark A. Schembri, Scott A. Beatson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4d65d87df14d45dfbd05858be1ed6786
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spelling	oai:doaj.org-article:4d65d87df14d45dfbd05858be1ed67862021-11-15T15:41:41ZSequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST13110.1128/mBio.00347-162150-7511https://doaj.org/article/4d65d87df14d45dfbd05858be1ed67862016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00347-16https://doaj.org/toc/2150-7511ABSTRACT Escherichia coli ST131 is the most frequently isolated fluoroquinolone-resistant (FQR) E. coli clone worldwide and a major cause of urinary tract and bloodstream infections. Although originally identified through its association with the CTX-M-15 extended-spectrum β-lactamase resistance gene, global genomic epidemiology studies have failed to resolve the geographical and temporal origin of the ST131 ancestor. Here, we developed a framework for the reanalysis of publically available genomes from different countries and used this data set to reconstruct the evolutionary steps that led to the emergence of FQR ST131. Using Bayesian estimation, we show that point mutations in chromosomal genes that confer FQR coincide with the first clinical use of fluoroquinolone in 1986 and illustrate the impact of this pivotal event on the rapid population expansion of ST131 worldwide from an apparent origin in North America. Furthermore, we identify virulence factor acquisition events that predate the development of FQR, suggesting that the gain of virulence-associated genes followed by the tandem development of antibiotic resistance primed the successful global dissemination of ST131. IMPORTANCE Escherichia coli sequence type 131 (ST131) is a recently emerged and globally disseminated multidrug-resistant clone frequently associated with human urinary tract and bloodstream infections. In this study, we have used two large publically available genomic data sets to define a number of critical steps in the evolution of this important pathogen. We show that resistance to fluoroquinolones, a class of broad-spectrum antibiotic used extensively in human medicine and veterinary practice, developed in ST131 soon after the introduction of these antibiotics in the United States, most likely in North America. We also mapped the acquisition of several fitness and virulence determinants by ST131 and demonstrate these events occurred prior to the development of fluoroquinolone resistance. Thus, ST131 has emerged by stealth, first acquiring genes associated with an increased capacity to cause human infection, and then gaining a resistance armory that has driven its massive population expansion across the globe.Nouri L. Ben ZakourAreej S. Alsheikh-HussainMelinda M. AshcroftNguyen Thi Khanh NhuLeah W. RobertsMitchell Stanton-CookMark A. SchembriScott A. BeatsonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Nouri L. Ben Zakour Areej S. Alsheikh-Hussain Melinda M. Ashcroft Nguyen Thi Khanh Nhu Leah W. Roberts Mitchell Stanton-Cook Mark A. Schembri Scott A. Beatson Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131
description	ABSTRACT Escherichia coli ST131 is the most frequently isolated fluoroquinolone-resistant (FQR) E. coli clone worldwide and a major cause of urinary tract and bloodstream infections. Although originally identified through its association with the CTX-M-15 extended-spectrum β-lactamase resistance gene, global genomic epidemiology studies have failed to resolve the geographical and temporal origin of the ST131 ancestor. Here, we developed a framework for the reanalysis of publically available genomes from different countries and used this data set to reconstruct the evolutionary steps that led to the emergence of FQR ST131. Using Bayesian estimation, we show that point mutations in chromosomal genes that confer FQR coincide with the first clinical use of fluoroquinolone in 1986 and illustrate the impact of this pivotal event on the rapid population expansion of ST131 worldwide from an apparent origin in North America. Furthermore, we identify virulence factor acquisition events that predate the development of FQR, suggesting that the gain of virulence-associated genes followed by the tandem development of antibiotic resistance primed the successful global dissemination of ST131. IMPORTANCE Escherichia coli sequence type 131 (ST131) is a recently emerged and globally disseminated multidrug-resistant clone frequently associated with human urinary tract and bloodstream infections. In this study, we have used two large publically available genomic data sets to define a number of critical steps in the evolution of this important pathogen. We show that resistance to fluoroquinolones, a class of broad-spectrum antibiotic used extensively in human medicine and veterinary practice, developed in ST131 soon after the introduction of these antibiotics in the United States, most likely in North America. We also mapped the acquisition of several fitness and virulence determinants by ST131 and demonstrate these events occurred prior to the development of fluoroquinolone resistance. Thus, ST131 has emerged by stealth, first acquiring genes associated with an increased capacity to cause human infection, and then gaining a resistance armory that has driven its massive population expansion across the globe.
format	article
author	Nouri L. Ben Zakour Areej S. Alsheikh-Hussain Melinda M. Ashcroft Nguyen Thi Khanh Nhu Leah W. Roberts Mitchell Stanton-Cook Mark A. Schembri Scott A. Beatson
author_facet	Nouri L. Ben Zakour Areej S. Alsheikh-Hussain Melinda M. Ashcroft Nguyen Thi Khanh Nhu Leah W. Roberts Mitchell Stanton-Cook Mark A. Schembri Scott A. Beatson
author_sort	Nouri L. Ben Zakour
title	Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131
title_short	Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131
title_full	Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131
title_fullStr	Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131
title_full_unstemmed	Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131
title_sort	sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of <named-content content-type="genus-species">escherichia coli</named-content> st131
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/4d65d87df14d45dfbd05858be1ed6786
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Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of <named-content content-type="genus-species">Escherichia coli</named-content> ST131

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