Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> 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 ExPEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully un...

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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Escherichia coli ST131 genomes plasmids Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b206e103a1094c0ea77ddb02dd996e7a
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spelling	oai:doaj.org-article:b206e103a1094c0ea77ddb02dd996e7a2021-11-15T15:21:14ZSeparate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 13110.1128/mSphere.00121-162379-5042https://doaj.org/article/b206e103a1094c0ea77ddb02dd996e7a2016-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00121-16https://doaj.org/toc/2379-5042ABSTRACT The extraintestinal pathogenic Escherichia coli (ExPEC) H30 subclone of sequence type 131 (ST131-H30) has emerged abruptly as a dominant lineage of ExPEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully understood. Here, single-molecule, 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. IMPORTANCE A clonal lineage of Escherichia coli known as ST131 has emerged as a dominating strain type causing extraintestinal infections in humans. The evolutionary history of ST131 E. coli is now well understood. However, the role of plasmids in ST131’s evolutionary history is poorly defined. This study utilized real-time, single-molecule sequencing to compare plasmids from various current and historical lineages of ST131. From this work, it was determined that a series of plasmid gains, losses, and recombinational events has led to the currently circulating plasmids of ST131 strains. These plasmids appear to have evolved to acquire similar gene clusters on multiple occasions, suggesting possible plasmid-mediated convergent evolution leading to evolutionary success. These plasmids also appear to be better suited to exist in specific strains of ST131 due to coadaptive mutations. Overall, a series of events has enabled the evolution of ST131 plasmids, possibly contributing to the lineage’s success.Timothy J. JohnsonJessica L. DanzeisenBonnie YoumansKyle CaseKatharine LlopJeannette Munoz-AguayoCristian Flores-FigueroaMaliha AzizNicole StoesserEvgeni SokurenkoLance B. PriceJames R. JohnsonAmerican Society for MicrobiologyarticleEscherichia coliST131genomesplasmidsMicrobiologyQR1-502ENmSphere, Vol 1, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli ST131 genomes plasmids Microbiology QR1-502
spellingShingle	Escherichia coli ST131 genomes plasmids Microbiology QR1-502 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 Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131
description	ABSTRACT The extraintestinal pathogenic Escherichia coli (ExPEC) H30 subclone of sequence type 131 (ST131-H30) has emerged abruptly as a dominant lineage of ExPEC responsible for human disease. The ST131-H30 lineage has been well described phylogenetically, yet its plasmid complement is not fully understood. Here, single-molecule, 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. IMPORTANCE A clonal lineage of Escherichia coli known as ST131 has emerged as a dominating strain type causing extraintestinal infections in humans. The evolutionary history of ST131 E. coli is now well understood. However, the role of plasmids in ST131’s evolutionary history is poorly defined. This study utilized real-time, single-molecule sequencing to compare plasmids from various current and historical lineages of ST131. From this work, it was determined that a series of plasmid gains, losses, and recombinational events has led to the currently circulating plasmids of ST131 strains. These plasmids appear to have evolved to acquire similar gene clusters on multiple occasions, suggesting possible plasmid-mediated convergent evolution leading to evolutionary success. These plasmids also appear to be better suited to exist in specific strains of ST131 due to coadaptive mutations. Overall, a series of events has enabled the evolution of ST131 plasmids, possibly contributing to the lineage’s success.
format	article
author	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
author_facet	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
author_sort	Timothy J. Johnson
title	Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131
title_short	Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131
title_full	Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131
title_fullStr	Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131
title_full_unstemmed	Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131
title_sort	separate f-type plasmids have shaped the evolution of the <italic toggle="yes">h</italic>30 subclone of <named-content content-type="genus-species">escherichia coli</named-content> sequence type 131
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/b206e103a1094c0ea77ddb02dd996e7a
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Separate F-Type Plasmids Have Shaped the Evolution of the <italic toggle="yes">H</italic>30 Subclone of <named-content content-type="genus-species">Escherichia coli</named-content> Sequence Type 131

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