Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131

Ben Zakour, Nouri L., Alsheikh-Hussain, Areej S., Ashcroft, Melinda M., Nhu, Nguyen Thi Khanh, Roberts, Leah W., Stanton-Cook, Mitchell, Schembri, Mark A. and Beatson, Scott A. (2016) Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131. MBio, 7 2: e00347-16.1-e00347-16.11. doi:10.1128/mBio.00347-16


Author Ben Zakour, Nouri L.
Alsheikh-Hussain, Areej S.
Ashcroft, Melinda M.
Nhu, Nguyen Thi Khanh
Roberts, Leah W.
Stanton-Cook, Mitchell
Schembri, Mark A.
Beatson, Scott A.
Title Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131
Formatted title
Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131
Journal name MBio   Check publisher's open access policy
ISSN 2150-7511
2161-2129
Publication date 2016-04-26
Sub-type Article (original research)
DOI 10.1128/mBio.00347-16
Open Access Status DOI
Volume 7
Issue 2
Start page e00347-16.1
End page e00347-16.11
Total pages 11
Place of publication Washington, DC, United States
Publisher American Society for Microbiology
Language eng
Formatted 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 CTXM- 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.
Q-Index Code C1
Q-Index Status Provisional Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: HERDC Pre-Audit
School of Chemistry and Molecular Biosciences
 
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Citation counts: TR Web of Science Citation Count  Cited 10 times in Thomson Reuters Web of Science Article | Citations
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Created: Fri, 06 May 2016, 20:46:55 EST by Mrs Louise Nimwegen on behalf of School of Chemistry & Molecular Biosciences