Separate F-type plasmids have shaped the evolution of the H30 subclone of Escherichia coli sequence type 131

Timothy J. Johnson; Jessica L. Danzeisen; Bonnie Youmans; Kyle Case; Katharine Llop; Jeannette Munoz-Aguayo; Cristian Flores-Figueroa; Maliha Aziz; Nicole Stoesser; Evgeni Sokurenko; Lance B. Price; James R. Johnson

doi:10.1128/mSphere.00121-16

Separate F-type plasmids have shaped the evolution of the H30 subclone of Escherichia coli sequence type 131

Timothy J. Johnson, Jessica L. Danzeisen, Bonnie Youmans, Kyle Case, Katharine Llop, Jeannette Munoz-Aguayo, Cristian Flores-Figueroa, Maliha Aziz, Nicole Stoesser, Evgeni Sokurenko, Lance B. Price, James R. Johnson

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Abstract

The extraintestinal pathogenic Escherichia coli (ExPEC) H30 subclone of sequence type 131 (ST131-H30) has emerged abruptly as a dominant lineage of Ex- PEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully understood. Here, singlemolecule, real-time sequencing was used to generate the complete plasmid sequences of ST131-H30 isolates and those belonging to other ST131 clades. Comparative analyses revealed separate F-type plasmids that have shaped the evolution of the main fluoroquinolone-resistant ST131-H30 clades. Specifically, an F1:A2:B20 plasmid is strongly associated with the H30R/C1 clade, whereas an F2:A1:B- plasmid is associated with the H30Rx/C2 clade. A series of plasmid gene losses, gains, and rearrangements involving IS26 likely led to the current plasmid complements within each ST131-H30 sublineage, which contain several overlapping gene clusters with putative functions in virulence and fitness, suggesting plasmid-mediated convergent evolution. Evidence suggests that the H30Rx/C2-associated F2:A1:B- plasmid type was present in strains ancestral to the acquisition of fluoroquinolone resistance and prior to the introduction of a multidrug resistance-encoding gene cassette harboring bla_CTX-M-15. In vitro experiments indicated a host strain-independent low frequency of plasmid transfer, differential levels of plasmid stability even between closely related ST131-H30 strains, and possible epistasis for carriage of these plasmids within the H30R/Rx lineages.

Original language	English (US)
Article number	e00121-16
Journal	mSphere
Volume	1
Issue number	4
DOIs	https://doi.org/10.1128/mSphere.00121-16
State	Published - Jul 1 2016

Bibliographical note

Funding Information:
This work was supported in part by University of Minnesota College of Veterinary Medicine funding. Computing resources were provided by the University of Minnesota Supercomputing Institute. This material also is based on work supported in part by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, grant no. 1 I01 CX000192 01 (J.R.J.), NIH grant no. R01AI106007 (E.S.), and NIH grant no. 2R21-AI117654 (L.B.P. and J.R.J.). N.S. is currently funded through a Public Health England/University of Oxford Clinical Lectureship. The opinions expressed here are strictly those of the authors and do not necessarily reflect those of their respective institutions or the Department of Veterans Affairs. This work, including the efforts of James R. Johnson, was funded by Office of Research and Development, VA (1 I01 CX000192 01). This work, including the efforts of Evgeni Sokurenko and Lance B. Price, was funded by HHS | National Institutes of Health (NIH) (R01AI106007 and 2R21-AI117654)

Publisher Copyright:
© 2016 Johnson et al.

Keywords

Escherichia coli
Genomes
Plasmids
ST131

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10.1128/mSphere.00121-16

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title = "Separate F-type plasmids have shaped the evolution of the H30 subclone of Escherichia coli sequence type 131",

abstract = "The extraintestinal pathogenic Escherichia coli (ExPEC) H30 subclone of sequence type 131 (ST131-H30) has emerged abruptly as a dominant lineage of Ex- PEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully understood. Here, singlemolecule, real-time sequencing was used to generate the complete plasmid sequences of ST131-H30 isolates and those belonging to other ST131 clades. Comparative analyses revealed separate F-type plasmids that have shaped the evolution of the main fluoroquinolone-resistant ST131-H30 clades. Specifically, an F1:A2:B20 plasmid is strongly associated with the H30R/C1 clade, whereas an F2:A1:B- plasmid is associated with the H30Rx/C2 clade. A series of plasmid gene losses, gains, and rearrangements involving IS26 likely led to the current plasmid complements within each ST131-H30 sublineage, which contain several overlapping gene clusters with putative functions in virulence and fitness, suggesting plasmid-mediated convergent evolution. Evidence suggests that the H30Rx/C2-associated F2:A1:B- plasmid type was present in strains ancestral to the acquisition of fluoroquinolone resistance and prior to the introduction of a multidrug resistance-encoding gene cassette harboring blaCTX-M-15. In vitro experiments indicated a host strain-independent low frequency of plasmid transfer, differential levels of plasmid stability even between closely related ST131-H30 strains, and possible epistasis for carriage of these plasmids within the H30R/Rx lineages.",

keywords = "Escherichia coli, Genomes, Plasmids, ST131",

author = "Johnson, {Timothy J.} and Danzeisen, {Jessica L.} and Bonnie Youmans and Kyle Case and Katharine Llop and Jeannette Munoz-Aguayo and Cristian Flores-Figueroa and Maliha Aziz and Nicole Stoesser and Evgeni Sokurenko and Price, {Lance B.} and Johnson, {James R.}",

note = "Funding Information: This work was supported in part by University of Minnesota College of Veterinary Medicine funding. Computing resources were provided by the University of Minnesota Supercomputing Institute. This material also is based on work supported in part by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, grant no. 1 I01 CX000192 01 (J.R.J.), NIH grant no. R01AI106007 (E.S.), and NIH grant no. 2R21-AI117654 (L.B.P. and J.R.J.). N.S. is currently funded through a Public Health England/University of Oxford Clinical Lectureship. The opinions expressed here are strictly those of the authors and do not necessarily reflect those of their respective institutions or the Department of Veterans Affairs. This work, including the efforts of James R. Johnson, was funded by Office of Research and Development, VA (1 I01 CX000192 01). This work, including the efforts of Evgeni Sokurenko and Lance B. Price, was funded by HHS | National Institutes of Health (NIH) (R01AI106007 and 2R21-AI117654) Publisher Copyright: {\textcopyright} 2016 Johnson et al.",

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doi = "10.1128/mSphere.00121-16",

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T1 - Separate F-type plasmids have shaped the evolution of the H30 subclone of Escherichia coli sequence type 131

AU - Johnson, Timothy J.

AU - Danzeisen, Jessica L.

AU - Youmans, Bonnie

AU - Case, Kyle

AU - Llop, Katharine

AU - Munoz-Aguayo, Jeannette

AU - Flores-Figueroa, Cristian

AU - Aziz, Maliha

AU - Stoesser, Nicole

AU - Sokurenko, Evgeni

AU - Price, Lance B.

AU - Johnson, James R.

N1 - Funding Information: This work was supported in part by University of Minnesota College of Veterinary Medicine funding. Computing resources were provided by the University of Minnesota Supercomputing Institute. This material also is based on work supported in part by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, grant no. 1 I01 CX000192 01 (J.R.J.), NIH grant no. R01AI106007 (E.S.), and NIH grant no. 2R21-AI117654 (L.B.P. and J.R.J.). N.S. is currently funded through a Public Health England/University of Oxford Clinical Lectureship. The opinions expressed here are strictly those of the authors and do not necessarily reflect those of their respective institutions or the Department of Veterans Affairs. This work, including the efforts of James R. Johnson, was funded by Office of Research and Development, VA (1 I01 CX000192 01). This work, including the efforts of Evgeni Sokurenko and Lance B. Price, was funded by HHS | National Institutes of Health (NIH) (R01AI106007 and 2R21-AI117654) Publisher Copyright: © 2016 Johnson et al.

PY - 2016/7/1

Y1 - 2016/7/1

N2 - The extraintestinal pathogenic Escherichia coli (ExPEC) H30 subclone of sequence type 131 (ST131-H30) has emerged abruptly as a dominant lineage of Ex- PEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully understood. Here, singlemolecule, real-time sequencing was used to generate the complete plasmid sequences of ST131-H30 isolates and those belonging to other ST131 clades. Comparative analyses revealed separate F-type plasmids that have shaped the evolution of the main fluoroquinolone-resistant ST131-H30 clades. Specifically, an F1:A2:B20 plasmid is strongly associated with the H30R/C1 clade, whereas an F2:A1:B- plasmid is associated with the H30Rx/C2 clade. A series of plasmid gene losses, gains, and rearrangements involving IS26 likely led to the current plasmid complements within each ST131-H30 sublineage, which contain several overlapping gene clusters with putative functions in virulence and fitness, suggesting plasmid-mediated convergent evolution. Evidence suggests that the H30Rx/C2-associated F2:A1:B- plasmid type was present in strains ancestral to the acquisition of fluoroquinolone resistance and prior to the introduction of a multidrug resistance-encoding gene cassette harboring blaCTX-M-15. In vitro experiments indicated a host strain-independent low frequency of plasmid transfer, differential levels of plasmid stability even between closely related ST131-H30 strains, and possible epistasis for carriage of these plasmids within the H30R/Rx lineages.

AB - The extraintestinal pathogenic Escherichia coli (ExPEC) H30 subclone of sequence type 131 (ST131-H30) has emerged abruptly as a dominant lineage of Ex- PEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully understood. Here, singlemolecule, real-time sequencing was used to generate the complete plasmid sequences of ST131-H30 isolates and those belonging to other ST131 clades. Comparative analyses revealed separate F-type plasmids that have shaped the evolution of the main fluoroquinolone-resistant ST131-H30 clades. Specifically, an F1:A2:B20 plasmid is strongly associated with the H30R/C1 clade, whereas an F2:A1:B- plasmid is associated with the H30Rx/C2 clade. A series of plasmid gene losses, gains, and rearrangements involving IS26 likely led to the current plasmid complements within each ST131-H30 sublineage, which contain several overlapping gene clusters with putative functions in virulence and fitness, suggesting plasmid-mediated convergent evolution. Evidence suggests that the H30Rx/C2-associated F2:A1:B- plasmid type was present in strains ancestral to the acquisition of fluoroquinolone resistance and prior to the introduction of a multidrug resistance-encoding gene cassette harboring blaCTX-M-15. In vitro experiments indicated a host strain-independent low frequency of plasmid transfer, differential levels of plasmid stability even between closely related ST131-H30 strains, and possible epistasis for carriage of these plasmids within the H30R/Rx lineages.

KW - Escherichia coli

KW - Genomes

KW - Plasmids

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Separate F-type plasmids have shaped the evolution of the H30 subclone of Escherichia coli sequence type 131

Abstract

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