Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection

ABSTRACT In the present study, it is shown that although Escherichia coli CFT073, a human uropathogenic (UPEC) strain, grows in liquid glucose M9 minimal medium, it fails to grow on glucose M9 minimal medium agar plates seeded with ≤106 CFU. The cells on glucose plates appear to be in a “quiescent”...

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Autores principales:	Mary P. Leatham-Jensen, Matthew E. Mokszycki, David C. Rowley, Robert Deering, Jodi L. Camberg, Evgeni V. Sokurenko, Veronika L. Tchesnokova, Jakob Frimodt-Møller, Karen A. Krogfelt, Karen Leth Nielsen, Niels Frimodt-Møller, Gongqin Sun, Paul S. Cohen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	E. coli quiescence E. coli persistence urinary tract infections carbon metabolism TCA cycle Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6497ab76beaa4d5e949dc9769acc0652
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spelling	oai:doaj.org-article:6497ab76beaa4d5e949dc9769acc06522021-11-15T15:21:37ZUropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection10.1128/mSphere.00055-152379-5042https://doaj.org/article/6497ab76beaa4d5e949dc9769acc06522016-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00055-15https://doaj.org/toc/2379-5042ABSTRACT In the present study, it is shown that although Escherichia coli CFT073, a human uropathogenic (UPEC) strain, grows in liquid glucose M9 minimal medium, it fails to grow on glucose M9 minimal medium agar plates seeded with ≤106 CFU. The cells on glucose plates appear to be in a “quiescent” state that can be prevented by various combinations of lysine, methionine, and tyrosine. Moreover, the quiescent state is characteristic of ~80% of E. coli phylogenetic group B2 multilocus sequence type 73 strains, as well as 22.5% of randomly selected UPEC strains isolated from community-acquired urinary tract infections in Denmark. In addition, E. coli CFT073 quiescence is not limited to glucose but occurs on agar plates containing a number of other sugars and acetate as sole carbon sources. It is also shown that a number of E. coli CFT073 mini-Tn5 metabolic mutants (gnd, gdhA, pykF, sdhA, and zwf) are nonquiescent on glucose M9 minimal agar plates and that quiescence requires a complete oxidative tricarboxylic acid (TCA) cycle. In addition, evidence is presented that, although E. coli CFT073 quiescence and persistence in the presence of ampicillin are alike in that both require a complete oxidative TCA cycle and each can be prevented by amino acids, E. coli CFT073 quiescence occurs in the presence or absence of a functional rpoS gene, whereas maximal persistence requires a nonfunctional rpoS. Our results suggest that interventions targeting specific central metabolic pathways may mitigate UPEC infections by interfering with quiescence and persistence. IMPORTANCE Recurrent urinary tract infections (UTIs) affect 10 to 40% of women. In up to 77% of those cases, the recurrent infections are caused by the same uropathogenic E. coli (UPEC) strain that caused the initial infection. Upon infection of urothelial transitional cells in the bladder, UPEC appear to enter a nongrowing quiescent intracellular state that is thought to serve as a reservoir responsible for recurrent UTIs. Here, we report that many UPEC strains enter a quiescent state when ≤106 CFU are seeded on glucose M9 minimal medium agar plates and show that mutations in several genes involved in central carbon metabolism prevent quiescence, as well as persistence, possibly identifying metabolic pathways involved in UPEC quiescence and persistence in vivo.Mary P. Leatham-JensenMatthew E. MokszyckiDavid C. RowleyRobert DeeringJodi L. CambergEvgeni V. SokurenkoVeronika L. TchesnokovaJakob Frimodt-MøllerKaren A. KrogfeltKaren Leth NielsenNiels Frimodt-MøllerGongqin SunPaul S. CohenAmerican Society for MicrobiologyarticleE. coli quiescenceE. coli persistenceurinary tract infectionscarbon metabolismTCA cycleMicrobiologyQR1-502ENmSphere, Vol 1, Iss 1 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	E. coli quiescence E. coli persistence urinary tract infections carbon metabolism TCA cycle Microbiology QR1-502
spellingShingle	E. coli quiescence E. coli persistence urinary tract infections carbon metabolism TCA cycle Microbiology QR1-502 Mary P. Leatham-Jensen Matthew E. Mokszycki David C. Rowley Robert Deering Jodi L. Camberg Evgeni V. Sokurenko Veronika L. Tchesnokova Jakob Frimodt-Møller Karen A. Krogfelt Karen Leth Nielsen Niels Frimodt-Møller Gongqin Sun Paul S. Cohen Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection
description	ABSTRACT In the present study, it is shown that although Escherichia coli CFT073, a human uropathogenic (UPEC) strain, grows in liquid glucose M9 minimal medium, it fails to grow on glucose M9 minimal medium agar plates seeded with ≤106 CFU. The cells on glucose plates appear to be in a “quiescent” state that can be prevented by various combinations of lysine, methionine, and tyrosine. Moreover, the quiescent state is characteristic of ~80% of E. coli phylogenetic group B2 multilocus sequence type 73 strains, as well as 22.5% of randomly selected UPEC strains isolated from community-acquired urinary tract infections in Denmark. In addition, E. coli CFT073 quiescence is not limited to glucose but occurs on agar plates containing a number of other sugars and acetate as sole carbon sources. It is also shown that a number of E. coli CFT073 mini-Tn5 metabolic mutants (gnd, gdhA, pykF, sdhA, and zwf) are nonquiescent on glucose M9 minimal agar plates and that quiescence requires a complete oxidative tricarboxylic acid (TCA) cycle. In addition, evidence is presented that, although E. coli CFT073 quiescence and persistence in the presence of ampicillin are alike in that both require a complete oxidative TCA cycle and each can be prevented by amino acids, E. coli CFT073 quiescence occurs in the presence or absence of a functional rpoS gene, whereas maximal persistence requires a nonfunctional rpoS. Our results suggest that interventions targeting specific central metabolic pathways may mitigate UPEC infections by interfering with quiescence and persistence. IMPORTANCE Recurrent urinary tract infections (UTIs) affect 10 to 40% of women. In up to 77% of those cases, the recurrent infections are caused by the same uropathogenic E. coli (UPEC) strain that caused the initial infection. Upon infection of urothelial transitional cells in the bladder, UPEC appear to enter a nongrowing quiescent intracellular state that is thought to serve as a reservoir responsible for recurrent UTIs. Here, we report that many UPEC strains enter a quiescent state when ≤106 CFU are seeded on glucose M9 minimal medium agar plates and show that mutations in several genes involved in central carbon metabolism prevent quiescence, as well as persistence, possibly identifying metabolic pathways involved in UPEC quiescence and persistence in vivo.
format	article
author	Mary P. Leatham-Jensen Matthew E. Mokszycki David C. Rowley Robert Deering Jodi L. Camberg Evgeni V. Sokurenko Veronika L. Tchesnokova Jakob Frimodt-Møller Karen A. Krogfelt Karen Leth Nielsen Niels Frimodt-Møller Gongqin Sun Paul S. Cohen
author_facet	Mary P. Leatham-Jensen Matthew E. Mokszycki David C. Rowley Robert Deering Jodi L. Camberg Evgeni V. Sokurenko Veronika L. Tchesnokova Jakob Frimodt-Møller Karen A. Krogfelt Karen Leth Nielsen Niels Frimodt-Møller Gongqin Sun Paul S. Cohen
author_sort	Mary P. Leatham-Jensen
title	Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection
title_short	Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection
title_full	Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection
title_fullStr	Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection
title_full_unstemmed	Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection
title_sort	uropathogenic <named-content content-type="genus-species">escherichia coli</named-content> metabolite-dependent quiescence and persistence may explain antibiotic tolerance during urinary tract infection
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/6497ab76beaa4d5e949dc9769acc0652
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Uropathogenic <named-content content-type="genus-species">Escherichia coli</named-content> Metabolite-Dependent Quiescence and Persistence May Explain Antibiotic Tolerance during Urinary Tract Infection

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