The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx
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)...
| Main Authors: | , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2013-12-01
|
| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00377-13 |
| _version_ | 1818856302381629440 |
|---|---|
| author | 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 Pearson Kim Riddell Peggy Rogers Delia Scholes Barbara Kahl Paul Keim Evgeni V. Sokurenko |
| author_facet | 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 Pearson Kim Riddell Peggy Rogers Delia Scholes Barbara Kahl Paul Keim Evgeni V. Sokurenko |
| author_sort | Lance B. Price |
| collection | DOAJ |
| description | 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-genome-sequence-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. IMPORTANCE We applied an advanced genomic approach to study the recent evolutionary history of one of the most important Escherichia coli strains in circulation today. This strain, called sequence type 131 (ST131), causes multidrug-resistant bladder, kidney, and bloodstream infections around the world. The rising prevalence of antibiotic resistance in E. coli is making these infections more difficult to treat and is leading to increased mortality. Past studies suggested that many different ST131 strains gained resistance to extended-spectrum cephalosporins independently. In contrast, our research indicates that most extended-spectrum-cephalosporin-resistant ST131 strains belong to a single highly pathogenic subclone, called H30-Rx. The clonal nature of H30-Rx may provide opportunities for vaccine or transmission prevention-based control strategies, which could gain importance as H30-Rx and other extraintestinal pathogenic E. coli subclones become resistant to our best antibiotics. |
| first_indexed | 2024-12-19T08:22:20Z |
| format | Article |
| id | doaj.art-525c39637cc54a2c8ee001a7adfd95e6 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T08:22:20Z |
| publishDate | 2013-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-525c39637cc54a2c8ee001a7adfd95e62022-12-21T20:29:22ZengAmerican Society for MicrobiologymBio2150-75112013-12-014610.1128/mBio.00377-13The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-RxLance B. Price0James R. Johnson1Maliha Aziz2Connie Clabots3Brian Johnston4Veronika Tchesnokova5Lora Nordstrom6Maria Billig7Sujay Chattopadhyay8Marc Stegger9Paal S. Andersen10Talima Pearson11Kim Riddell12Peggy Rogers13Delia Scholes14Barbara Kahl15Paul Keim16Evgeni V. Sokurenko17Division of Pathogen Genomics, the Translational Genomics Research Institute, Flagstaff, Arizona, USAVeterans Affairs Medical Center and University of Minnesota, Minneapolis, Minnesota, USADivision of Pathogen Genomics, the Translational Genomics Research Institute, Flagstaff, Arizona, USAVeterans Affairs Medical Center and University of Minnesota, Minneapolis, Minnesota, USAVeterans Affairs Medical Center and University of Minnesota, Minneapolis, Minnesota, USADepartment of Microbiology, University of Washington School of Medicine, Seattle, Washington, USADepartment of Occupational and Environmental Health, George Washington University, Washington, DC, USADepartment of Microbiology, University of Washington School of Medicine, Seattle, Washington, USADepartment of Microbiology, University of Washington School of Medicine, Seattle, Washington, USADivision of Pathogen Genomics, the Translational Genomics Research Institute, Flagstaff, Arizona, USADivision of Pathogen Genomics, the Translational Genomics Research Institute, Flagstaff, Arizona, USACenter for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USAGroup Health Clinical Laboratory, Group Health Cooperative, Seattle, Washington, USAGroup Health Clinical Laboratory, Group Health Cooperative, Seattle, Washington, USAGroup Health Research Institute, Group Health Cooperative, Seattle, Washington, USAInstitute of Medical Microbiology, Universitätsklinikum Munster, Münster, GermanyDivision of Pathogen Genomics, the Translational Genomics Research Institute, Flagstaff, Arizona, USADepartment of Microbiology, University of Washington School of Medicine, Seattle, Washington, USAABSTRACT 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-genome-sequence-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. IMPORTANCE We applied an advanced genomic approach to study the recent evolutionary history of one of the most important Escherichia coli strains in circulation today. This strain, called sequence type 131 (ST131), causes multidrug-resistant bladder, kidney, and bloodstream infections around the world. The rising prevalence of antibiotic resistance in E. coli is making these infections more difficult to treat and is leading to increased mortality. Past studies suggested that many different ST131 strains gained resistance to extended-spectrum cephalosporins independently. In contrast, our research indicates that most extended-spectrum-cephalosporin-resistant ST131 strains belong to a single highly pathogenic subclone, called H30-Rx. The clonal nature of H30-Rx may provide opportunities for vaccine or transmission prevention-based control strategies, which could gain importance as H30-Rx and other extraintestinal pathogenic E. coli subclones become resistant to our best antibiotics.https://journals.asm.org/doi/10.1128/mBio.00377-13 |
| spellingShingle | 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 Pearson Kim Riddell Peggy Rogers Delia Scholes Barbara Kahl Paul Keim Evgeni V. Sokurenko The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx mBio |
| title | The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx |
| title_full | The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx |
| title_fullStr | The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx |
| title_full_unstemmed | The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx |
| title_short | The Epidemic of Extended-Spectrum-β-Lactamase-Producing <named-content content-type="genus-species">Escherichia coli</named-content> ST131 Is Driven by a Single Highly Pathogenic Subclone, <italic toggle="yes">H</italic>30-Rx |
| title_sort | epidemic of extended spectrum β lactamase producing named content content type genus species escherichia coli named content st131 is driven by a single highly pathogenic subclone italic toggle yes h italic 30 rx |
| url | https://journals.asm.org/doi/10.1128/mBio.00377-13 |
| work_keys_str_mv | AT lancebprice theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT jamesrjohnson theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT malihaaziz theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT connieclabots theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT brianjohnston theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT veronikatchesnokova theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT loranordstrom theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT mariabillig theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT sujaychattopadhyay theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT marcstegger theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT paalsandersen theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT talimapearson theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT kimriddell theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT peggyrogers theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT deliascholes theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT barbarakahl theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT paulkeim theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT evgenivsokurenko theepidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT lancebprice epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT jamesrjohnson epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT malihaaziz epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT connieclabots epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT brianjohnston epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT veronikatchesnokova epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT loranordstrom epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT mariabillig epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT sujaychattopadhyay epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT marcstegger epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT paalsandersen epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT talimapearson epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT kimriddell epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT peggyrogers epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT deliascholes epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT barbarakahl epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT paulkeim epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx AT evgenivsokurenko epidemicofextendedspectrumblactamaseproducingnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentst131isdrivenbyasinglehighlypathogenicsubcloneitalictoggleyeshitalic30rx |