Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid

ABSTRACT The two-component system TctD-TctE is important for regulating the uptake of tricarboxylic acids in Pseudomonas aeruginosa. TctD-TctE accomplishes this through derepression of the gene opdH, which encodes a tricarboxylic acid-specific porin. Previous work from our lab revealed that TctD-Tct...

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Autores principales:	Patrick K. Taylor, Li Zhang, Thien-Fah Mah
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Pseudomonas aeruginosa biofilms citric acid two-component regulatory systems Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4219bd99b4384b2e9bdaf0a40ed5303b
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spelling	oai:doaj.org-article:4219bd99b4384b2e9bdaf0a40ed5303b2021-11-15T15:22:22ZLoss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid10.1128/mSphere.00102-192379-5042https://doaj.org/article/4219bd99b4384b2e9bdaf0a40ed5303b2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00102-19https://doaj.org/toc/2379-5042ABSTRACT The two-component system TctD-TctE is important for regulating the uptake of tricarboxylic acids in Pseudomonas aeruginosa. TctD-TctE accomplishes this through derepression of the gene opdH, which encodes a tricarboxylic acid-specific porin. Previous work from our lab revealed that TctD-TctE in P. aeruginosa also has a role in resistance to aminoglycoside antibiotics. The aim of this study was to further characterize the role of TctD-TctE in P. aeruginosa in the presence of citric acid. Here it was found that deletion of P. aeruginosa PA14 TctD-TctE (ΔtctED) resulted in a 4-fold decrease in the biofilm bactericidal concentrations of the aminoglycosides tobramycin and gentamicin when citric acid was present in nutrient media. Tobramycin accumulation assays demonstrated that deletion of TctD-TctE resulted in an increase in the amount of tobramycin retained in biofilm cells. The PA14 wild type responded to increasing concentrations of citric acid by producing less biofilm. In contrast, the amount of ΔtctED mutant biofilm formation remained constant or enhanced. Furthermore, the ΔtctED strain was incapable of growing on citric acid as a sole carbon source and was highly reduced in its ability to grow in the presence of citric acid even when an additional carbon source was available. Use of phenotypic and genetic microarrays found that this growth deficiency of the ΔtctED mutant is unique to citric acid and that multiple metabolic genes are dysregulated. This work demonstrates that TctD-TctE in P. aeruginosa has a role in biofilm development that is dependent on citric acid and that is separate from the previously characterized involvement in resistance to antibiotics. IMPORTANCE Nutrient availability is an important contributor to the ability of bacteria to establish successful infections in a host. Pseudomonas aeruginosa is an opportunistic pathogen in humans causing infections that are difficult to treat. In part, its success is attributable to a high degree of metabolic versatility. P. aeruginosa is able to sense and respond to varied and limited nutrient stress in the host environment. Two-component systems are important sensors-regulators of cellular responses to environmental stresses, such as those encountered in the host. This work demonstrates that the response by the two-component system TctD-TctE to the presence of citric acid has a role in biofilm formation, aminoglycoside susceptibility, and growth in P. aeruginosa.Patrick K. TaylorLi ZhangThien-Fah MahAmerican Society for MicrobiologyarticlePseudomonas aeruginosabiofilmscitric acidtwo-component regulatory systemsMicrobiologyQR1-502ENmSphere, Vol 4, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa biofilms citric acid two-component regulatory systems Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa biofilms citric acid two-component regulatory systems Microbiology QR1-502 Patrick K. Taylor Li Zhang Thien-Fah Mah Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid
description	ABSTRACT The two-component system TctD-TctE is important for regulating the uptake of tricarboxylic acids in Pseudomonas aeruginosa. TctD-TctE accomplishes this through derepression of the gene opdH, which encodes a tricarboxylic acid-specific porin. Previous work from our lab revealed that TctD-TctE in P. aeruginosa also has a role in resistance to aminoglycoside antibiotics. The aim of this study was to further characterize the role of TctD-TctE in P. aeruginosa in the presence of citric acid. Here it was found that deletion of P. aeruginosa PA14 TctD-TctE (ΔtctED) resulted in a 4-fold decrease in the biofilm bactericidal concentrations of the aminoglycosides tobramycin and gentamicin when citric acid was present in nutrient media. Tobramycin accumulation assays demonstrated that deletion of TctD-TctE resulted in an increase in the amount of tobramycin retained in biofilm cells. The PA14 wild type responded to increasing concentrations of citric acid by producing less biofilm. In contrast, the amount of ΔtctED mutant biofilm formation remained constant or enhanced. Furthermore, the ΔtctED strain was incapable of growing on citric acid as a sole carbon source and was highly reduced in its ability to grow in the presence of citric acid even when an additional carbon source was available. Use of phenotypic and genetic microarrays found that this growth deficiency of the ΔtctED mutant is unique to citric acid and that multiple metabolic genes are dysregulated. This work demonstrates that TctD-TctE in P. aeruginosa has a role in biofilm development that is dependent on citric acid and that is separate from the previously characterized involvement in resistance to antibiotics. IMPORTANCE Nutrient availability is an important contributor to the ability of bacteria to establish successful infections in a host. Pseudomonas aeruginosa is an opportunistic pathogen in humans causing infections that are difficult to treat. In part, its success is attributable to a high degree of metabolic versatility. P. aeruginosa is able to sense and respond to varied and limited nutrient stress in the host environment. Two-component systems are important sensors-regulators of cellular responses to environmental stresses, such as those encountered in the host. This work demonstrates that the response by the two-component system TctD-TctE to the presence of citric acid has a role in biofilm formation, aminoglycoside susceptibility, and growth in P. aeruginosa.
format	article
author	Patrick K. Taylor Li Zhang Thien-Fah Mah
author_facet	Patrick K. Taylor Li Zhang Thien-Fah Mah
author_sort	Patrick K. Taylor
title	Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid
title_short	Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid
title_full	Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid
title_fullStr	Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid
title_full_unstemmed	Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid
title_sort	loss of the two-component system tctd-tcte in <italic toggle="yes">pseudomonas aeruginosa</italic> affects biofilm formation and aminoglycoside susceptibility in response to citric acid
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/4219bd99b4384b2e9bdaf0a40ed5303b
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Loss of the Two-Component System TctD-TctE in <italic toggle="yes">Pseudomonas aeruginosa</italic> Affects Biofilm Formation and Aminoglycoside Susceptibility in Response to Citric Acid

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