The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx

Lance B. Price, James R. Johnson, Maliha Aziz, Connie Clabots, Brian Johnston, Veronika Tchesnokova, Lora Nordstrom, Maria Billig, Sujay Chattopadhyay, Marc Stegger, Paal S. Andersen, Talima R Pearson, Kim Riddell, Peggy Rogers, Delia Scholes, Barbara Kahl, Paul S Keim, Evgeni V. Sokurenko

Research output: Contribution to journalArticle

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Abstract

The Escherichia coli sequence type 131 (ST131) clone is notorious for extraintestinal infections, fluoroquinolone resistance, and extended-spectrum beta-lactamase (ESBL) production, attributable to a CTX-M-15-encoding mobile element. Here, we applied pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing to reconstruct the evolutionary history of the ST131 clone. PFGE-based cluster analyses suggested that both fluoroquinolone resistance and ESBL production had been acquired by multiple ST131 sublineages through independent genetic events. In contrast, the more robust whole-genomesequence-based phylogenomic analysis revealed that fluoroquinolone resistance was confined almost entirely to a single, rapidly expanding ST131 subclone, designated H30-R. Strikingly, 91% of the CTX-M-15-producing isolates also belonged to a single, well-defined clade nested within H30-R, which was named H30-Rx due to its more extensive resistance. Despite its tight clonal relationship with H30Rx, the CTX-M-15 mobile element was inserted variably in plasmid and chromosomal locations within the H30-Rx genome. Screening of a large collection of recent clinical E. coli isolates both confirmed the global clonal expansion of H30-Rx and revealed its disproportionate association with sepsis (relative risk, 7.5; P < 0.001). Together, these results suggest that the high prevalence of CTX-M-15 production among ST131 isolates is due primarily to the expansion of a single, highly virulent subclone, H30-Rx.

Original languageEnglish (US)
Article numbere00377-13
JournalmBio
Volume4
Issue number6
DOIs
StatePublished - Dec 17 2013

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Fluoroquinolones
Escherichia coli
Pulsed Field Gel Electrophoresis
beta-Lactamases
Clone Cells
Genome
Cluster Analysis
Sepsis
Plasmids
History
galantide
Infection

ASJC Scopus subject areas

  • Microbiology
  • Virology
  • Medicine(all)

Cite this

Price, L. B., Johnson, J. R., Aziz, M., Clabots, C., Johnston, B., Tchesnokova, V., ... Sokurenko, E. V. (2013). The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio, 4(6), [e00377-13]. https://doi.org/10.1128/mBio.00377-13

The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. / Price, Lance B.; Johnson, James R.; Aziz, Maliha; Clabots, Connie; Johnston, Brian; Tchesnokova, Veronika; Nordstrom, Lora; Billig, Maria; Chattopadhyay, Sujay; Stegger, Marc; Andersen, Paal S.; Pearson, Talima R; Riddell, Kim; Rogers, Peggy; Scholes, Delia; Kahl, Barbara; Keim, Paul S; Sokurenko, Evgeni V.

In: mBio, Vol. 4, No. 6, e00377-13, 17.12.2013.

Research output: Contribution to journalArticle

Price, LB, Johnson, JR, Aziz, M, Clabots, C, Johnston, B, Tchesnokova, V, Nordstrom, L, Billig, M, Chattopadhyay, S, Stegger, M, Andersen, PS, Pearson, TR, Riddell, K, Rogers, P, Scholes, D, Kahl, B, Keim, PS & Sokurenko, EV 2013, 'The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx', mBio, vol. 4, no. 6, e00377-13. https://doi.org/10.1128/mBio.00377-13
Price, Lance B. ; Johnson, James R. ; Aziz, Maliha ; Clabots, Connie ; Johnston, Brian ; Tchesnokova, Veronika ; Nordstrom, Lora ; Billig, Maria ; Chattopadhyay, Sujay ; Stegger, Marc ; Andersen, Paal S. ; Pearson, Talima R ; Riddell, Kim ; Rogers, Peggy ; Scholes, Delia ; Kahl, Barbara ; Keim, Paul S ; Sokurenko, Evgeni V. / The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. In: mBio. 2013 ; Vol. 4, No. 6.
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abstract = "The Escherichia coli sequence type 131 (ST131) clone is notorious for extraintestinal infections, fluoroquinolone resistance, and extended-spectrum beta-lactamase (ESBL) production, attributable to a CTX-M-15-encoding mobile element. Here, we applied pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing to reconstruct the evolutionary history of the ST131 clone. PFGE-based cluster analyses suggested that both fluoroquinolone resistance and ESBL production had been acquired by multiple ST131 sublineages through independent genetic events. In contrast, the more robust whole-genomesequence-based phylogenomic analysis revealed that fluoroquinolone resistance was confined almost entirely to a single, rapidly expanding ST131 subclone, designated H30-R. Strikingly, 91{\%} of the CTX-M-15-producing isolates also belonged to a single, well-defined clade nested within H30-R, which was named H30-Rx due to its more extensive resistance. Despite its tight clonal relationship with H30Rx, the CTX-M-15 mobile element was inserted variably in plasmid and chromosomal locations within the H30-Rx genome. Screening of a large collection of recent clinical E. coli isolates both confirmed the global clonal expansion of H30-Rx and revealed its disproportionate association with sepsis (relative risk, 7.5; P < 0.001). Together, these results suggest that the high prevalence of CTX-M-15 production among ST131 isolates is due primarily to the expansion of a single, highly virulent subclone, H30-Rx.",
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AU - Johnson, James R.

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AU - Johnston, Brian

AU - Tchesnokova, Veronika

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AU - Chattopadhyay, Sujay

AU - Stegger, Marc

AU - Andersen, Paal S.

AU - Pearson, Talima R

AU - Riddell, Kim

AU - Rogers, Peggy

AU - Scholes, Delia

AU - Kahl, Barbara

AU - Keim, Paul S

AU - Sokurenko, Evgeni V.

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N2 - The Escherichia coli sequence type 131 (ST131) clone is notorious for extraintestinal infections, fluoroquinolone resistance, and extended-spectrum beta-lactamase (ESBL) production, attributable to a CTX-M-15-encoding mobile element. Here, we applied pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing to reconstruct the evolutionary history of the ST131 clone. PFGE-based cluster analyses suggested that both fluoroquinolone resistance and ESBL production had been acquired by multiple ST131 sublineages through independent genetic events. In contrast, the more robust whole-genomesequence-based phylogenomic analysis revealed that fluoroquinolone resistance was confined almost entirely to a single, rapidly expanding ST131 subclone, designated H30-R. Strikingly, 91% of the CTX-M-15-producing isolates also belonged to a single, well-defined clade nested within H30-R, which was named H30-Rx due to its more extensive resistance. Despite its tight clonal relationship with H30Rx, the CTX-M-15 mobile element was inserted variably in plasmid and chromosomal locations within the H30-Rx genome. Screening of a large collection of recent clinical E. coli isolates both confirmed the global clonal expansion of H30-Rx and revealed its disproportionate association with sepsis (relative risk, 7.5; P < 0.001). Together, these results suggest that the high prevalence of CTX-M-15 production among ST131 isolates is due primarily to the expansion of a single, highly virulent subclone, H30-Rx.

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