Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages

ABSTRACT Multidrug-resistant (MDR) Escherichia coli strains are a major global threat to human health, wherein multidrug resistance is primarily spread by MDR plasmid acquisition. MDR plasmids are not widely distributed across the entire E. coli species, but instead are concentrated in a small numbe...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Steven Dunn, Laura Carrilero, Michael Brockhurst, Alan McNally
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Escherichia coli transcriptomics antimicrobial resistance plasmids Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/65a03b606d4b42bbb7adb9779a0d9f51
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:65a03b606d4b42bbb7adb9779a0d9f51
record_format	dspace
spelling	oai:doaj.org-article:65a03b606d4b42bbb7adb9779a0d9f512021-12-02T19:36:40ZLimited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages10.1128/mSystems.00083-212379-5077https://doaj.org/article/65a03b606d4b42bbb7adb9779a0d9f512021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00083-21https://doaj.org/toc/2379-5077ABSTRACT Multidrug-resistant (MDR) Escherichia coli strains are a major global threat to human health, wherein multidrug resistance is primarily spread by MDR plasmid acquisition. MDR plasmids are not widely distributed across the entire E. coli species, but instead are concentrated in a small number of clones. Here, we test if diverse E. coli strains vary in their ability to acquire and maintain MDR plasmids and if this relates to their transcriptional response following plasmid acquisition. We used strains from across the diversity of E. coli strains, including the common MDR lineage sequence type 131 (ST131) and the IncF plasmid pLL35, carrying multiple antibiotic resistance genes. Strains varied in their ability to acquire pLL35 by conjugation, but all were able to stably maintain the plasmid. The effects of pLL35 acquisition on cefotaxime resistance and growth also varied among strains, with growth responses ranging from a small decrease to a small increase in growth of the plasmid carrier relative to the parental strain. Transcriptional responses to pLL35 acquisition were limited in scale and highly strain specific. We observed transcriptional responses at the operon or regulon level—possibly due to stress responses or interactions with resident mobile genetic elements (MGEs). Subtle transcriptional responses consistent across all strains were observed affecting functions, such as anaerobic metabolism, previously shown to be under negative frequency-dependent selection in MDR E. coli. Overall, there was no correlation between the magnitudes of the transcriptional and growth responses across strains. Together, these data suggest that fitness costs arising from transcriptional disruption are unlikely to act as a barrier to dissemination of this MDR plasmid in E. coli. IMPORTANCE Plasmids play a key role in bacterial evolution by transferring adaptive functions between lineages that often enable invasion of new niches, including driving the spread of antibiotic resistance genes. Fitness costs of plasmid acquisition arising from the disruption of cellular processes could limit the spread of multidrug resistance plasmids. However, the impacts of plasmid acquisition are typically measured in lab-adapted strains rather than natural isolates, which act as reservoirs for the maintenance and transmission of plasmids to clinically relevant strains. Using a clinical multidrug resistance plasmid and a diverse collection of E. coli strains isolated from clinical infections and natural environments, we show that plasmid acquisition had only limited and highly strain-specific effects on bacterial growth and transcription under laboratory conditions. These findings suggest that fitness costs arising from transcriptional disruption are unlikely to act as a barrier to transmission of this plasmid in natural populations of E. coli.Steven DunnLaura CarrileroMichael BrockhurstAlan McNallyAmerican Society for MicrobiologyarticleEscherichia colitranscriptomicsantimicrobial resistanceplasmidsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli transcriptomics antimicrobial resistance plasmids Microbiology QR1-502
spellingShingle	Escherichia coli transcriptomics antimicrobial resistance plasmids Microbiology QR1-502 Steven Dunn Laura Carrilero Michael Brockhurst Alan McNally Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages
description	ABSTRACT Multidrug-resistant (MDR) Escherichia coli strains are a major global threat to human health, wherein multidrug resistance is primarily spread by MDR plasmid acquisition. MDR plasmids are not widely distributed across the entire E. coli species, but instead are concentrated in a small number of clones. Here, we test if diverse E. coli strains vary in their ability to acquire and maintain MDR plasmids and if this relates to their transcriptional response following plasmid acquisition. We used strains from across the diversity of E. coli strains, including the common MDR lineage sequence type 131 (ST131) and the IncF plasmid pLL35, carrying multiple antibiotic resistance genes. Strains varied in their ability to acquire pLL35 by conjugation, but all were able to stably maintain the plasmid. The effects of pLL35 acquisition on cefotaxime resistance and growth also varied among strains, with growth responses ranging from a small decrease to a small increase in growth of the plasmid carrier relative to the parental strain. Transcriptional responses to pLL35 acquisition were limited in scale and highly strain specific. We observed transcriptional responses at the operon or regulon level—possibly due to stress responses or interactions with resident mobile genetic elements (MGEs). Subtle transcriptional responses consistent across all strains were observed affecting functions, such as anaerobic metabolism, previously shown to be under negative frequency-dependent selection in MDR E. coli. Overall, there was no correlation between the magnitudes of the transcriptional and growth responses across strains. Together, these data suggest that fitness costs arising from transcriptional disruption are unlikely to act as a barrier to dissemination of this MDR plasmid in E. coli. IMPORTANCE Plasmids play a key role in bacterial evolution by transferring adaptive functions between lineages that often enable invasion of new niches, including driving the spread of antibiotic resistance genes. Fitness costs of plasmid acquisition arising from the disruption of cellular processes could limit the spread of multidrug resistance plasmids. However, the impacts of plasmid acquisition are typically measured in lab-adapted strains rather than natural isolates, which act as reservoirs for the maintenance and transmission of plasmids to clinically relevant strains. Using a clinical multidrug resistance plasmid and a diverse collection of E. coli strains isolated from clinical infections and natural environments, we show that plasmid acquisition had only limited and highly strain-specific effects on bacterial growth and transcription under laboratory conditions. These findings suggest that fitness costs arising from transcriptional disruption are unlikely to act as a barrier to transmission of this plasmid in natural populations of E. coli.
format	article
author	Steven Dunn Laura Carrilero Michael Brockhurst Alan McNally
author_facet	Steven Dunn Laura Carrilero Michael Brockhurst Alan McNally
author_sort	Steven Dunn
title	Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages
title_short	Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages
title_full	Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages
title_fullStr	Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages
title_full_unstemmed	Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages
title_sort	limited and strain-specific transcriptional and growth responses to acquisition of a multidrug resistance plasmid in genetically diverse <named-content content-type="genus-species">escherichia coli</named-content> lineages
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/65a03b606d4b42bbb7adb9779a0d9f51
work_keys_str_mv	AT stevendunn limitedandstrainspecifictranscriptionalandgrowthresponsestoacquisitionofamultidrugresistanceplasmidingeneticallydiversenamedcontentcontenttypegenusspeciesescherichiacolinamedcontentlineages AT lauracarrilero limitedandstrainspecifictranscriptionalandgrowthresponsestoacquisitionofamultidrugresistanceplasmidingeneticallydiversenamedcontentcontenttypegenusspeciesescherichiacolinamedcontentlineages AT michaelbrockhurst limitedandstrainspecifictranscriptionalandgrowthresponsestoacquisitionofamultidrugresistanceplasmidingeneticallydiversenamedcontentcontenttypegenusspeciesescherichiacolinamedcontentlineages AT alanmcnally limitedandstrainspecifictranscriptionalandgrowthresponsestoacquisitionofamultidrugresistanceplasmidingeneticallydiversenamedcontentcontenttypegenusspeciesescherichiacolinamedcontentlineages
_version_	1718376325644812288

Limited and Strain-Specific Transcriptional and Growth Responses to Acquisition of a Multidrug Resistance Plasmid in Genetically Diverse <named-content content-type="genus-species">Escherichia coli</named-content> Lineages

Ejemplares similares