Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection

ABSTRACT The urinary tract is one of the most frequent sites of bacterial infection in humans. Uropathogenic Escherichia coli (UPEC) strains are the leading cause of urinary tract infections (UTIs) and are responsible for greater than 80% of uncomplicated cases in adults. Infection of the urinary tr...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Matthew S. Walters, M. Chelsea Lane, Patrick D. Vigil, Sara N. Smith, Seth T. Walk, Harry L. T. Mobley
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2012
Materias:
Acceso en línea:https://doaj.org/article/24d3c2c87f014b66a4392a6e642af90d
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:24d3c2c87f014b66a4392a6e642af90d
record_format dspace
spelling oai:doaj.org-article:24d3c2c87f014b66a4392a6e642af90d2021-11-15T15:39:02ZKinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection10.1128/mBio.00303-112150-7511https://doaj.org/article/24d3c2c87f014b66a4392a6e642af90d2012-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00303-11https://doaj.org/toc/2150-7511ABSTRACT The urinary tract is one of the most frequent sites of bacterial infection in humans. Uropathogenic Escherichia coli (UPEC) strains are the leading cause of urinary tract infections (UTIs) and are responsible for greater than 80% of uncomplicated cases in adults. Infection of the urinary tract occurs in an ascending manner, with colonization of the bladder leading to possible kidney infection and bacteremia. The goal of this study was to examine the population dynamics of UPEC in vivo using a murine model of ascending UTI. To track individual UPEC lineages within a host, we constructed 10 isogenic clones of UPEC strain CFT073 by inserting unique signature tag sequences between the pstS and glmS genes at the attTn7 chromosomal site. Mice were transurethrally inoculated with a mixture containing equal numbers of unique clones. After 4 and 48 h, the tags present in the bladders, kidneys, and spleens of infected mice were enumerated using tag-specific primers and quantitative real-time PCR. The results indicated that kidney infection and bacteremia associated with UTI are most likely the result of multiple rounds of ascension and dissemination from motile UPEC subpopulations, with a distinct bottleneck existing between the kidney and bloodstream. The abundance of tagged lineages became more variable as infection progressed, especially after bacterial ascension to the upper urinary tract. Analysis of the population kinetics of UPEC during UTI revealed metapopulation dynamics, with lineages that constantly increased and decreased in abundance as they migrated from one organ to another. IMPORTANCE Urinary tract infections are some of the most common infections affecting humans, and Escherichia coli is the primary cause in most uncomplicated cases. These infections occur in an ascending manner, with bacteria traveling from the bladder to the kidneys and potentially the bloodstream. Little is known about the spatiotemporal population dynamics of uropathogenic E. coli within a host. Here we describe a novel approach for tracking lineages of isogenic tagged E. coli strains within a murine host by the use of quantitative real-time PCR. Understanding the in vivo population dynamics and the factors that shape the bacterial population may prove to be of significant value in the development of novel vaccines and drug therapies.Matthew S. WaltersM. Chelsea LanePatrick D. VigilSara N. SmithSeth T. WalkHarry L. T. MobleyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 1 (2012)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Matthew S. Walters
M. Chelsea Lane
Patrick D. Vigil
Sara N. Smith
Seth T. Walk
Harry L. T. Mobley
Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection
description ABSTRACT The urinary tract is one of the most frequent sites of bacterial infection in humans. Uropathogenic Escherichia coli (UPEC) strains are the leading cause of urinary tract infections (UTIs) and are responsible for greater than 80% of uncomplicated cases in adults. Infection of the urinary tract occurs in an ascending manner, with colonization of the bladder leading to possible kidney infection and bacteremia. The goal of this study was to examine the population dynamics of UPEC in vivo using a murine model of ascending UTI. To track individual UPEC lineages within a host, we constructed 10 isogenic clones of UPEC strain CFT073 by inserting unique signature tag sequences between the pstS and glmS genes at the attTn7 chromosomal site. Mice were transurethrally inoculated with a mixture containing equal numbers of unique clones. After 4 and 48 h, the tags present in the bladders, kidneys, and spleens of infected mice were enumerated using tag-specific primers and quantitative real-time PCR. The results indicated that kidney infection and bacteremia associated with UTI are most likely the result of multiple rounds of ascension and dissemination from motile UPEC subpopulations, with a distinct bottleneck existing between the kidney and bloodstream. The abundance of tagged lineages became more variable as infection progressed, especially after bacterial ascension to the upper urinary tract. Analysis of the population kinetics of UPEC during UTI revealed metapopulation dynamics, with lineages that constantly increased and decreased in abundance as they migrated from one organ to another. IMPORTANCE Urinary tract infections are some of the most common infections affecting humans, and Escherichia coli is the primary cause in most uncomplicated cases. These infections occur in an ascending manner, with bacteria traveling from the bladder to the kidneys and potentially the bloodstream. Little is known about the spatiotemporal population dynamics of uropathogenic E. coli within a host. Here we describe a novel approach for tracking lineages of isogenic tagged E. coli strains within a murine host by the use of quantitative real-time PCR. Understanding the in vivo population dynamics and the factors that shape the bacterial population may prove to be of significant value in the development of novel vaccines and drug therapies.
format article
author Matthew S. Walters
M. Chelsea Lane
Patrick D. Vigil
Sara N. Smith
Seth T. Walk
Harry L. T. Mobley
author_facet Matthew S. Walters
M. Chelsea Lane
Patrick D. Vigil
Sara N. Smith
Seth T. Walk
Harry L. T. Mobley
author_sort Matthew S. Walters
title Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection
title_short Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection
title_full Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection
title_fullStr Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection
title_full_unstemmed Kinetics of Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metapopulation Movement during Urinary Tract Infection
title_sort kinetics of uropathogenic <named-content content-type="genus-species">escherichia coli</named-content> metapopulation movement during urinary tract infection
publisher American Society for Microbiology
publishDate 2012
url https://doaj.org/article/24d3c2c87f014b66a4392a6e642af90d
work_keys_str_mv AT matthewswalters kineticsofuropathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmetapopulationmovementduringurinarytractinfection
AT mchelsealane kineticsofuropathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmetapopulationmovementduringurinarytractinfection
AT patrickdvigil kineticsofuropathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmetapopulationmovementduringurinarytractinfection
AT saransmith kineticsofuropathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmetapopulationmovementduringurinarytractinfection
AT sethtwalk kineticsofuropathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmetapopulationmovementduringurinarytractinfection
AT harryltmobley kineticsofuropathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmetapopulationmovementduringurinarytractinfection
_version_ 1718427753322119168