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Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae

The transmissible locus of stress tolerance (tLST) is a genomic island which confers resistance to heat and chlorine. In this study, we determined that the tLST is frequent in genomes of those Enterobacteriaceae that occur in association with plants as well as the intestines of humans and animals an...

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Autores principales: Wang, Zhiying, Hu, Huifeng, Zhu, Tongbo, Zheng, Jinshui, Gänzle, Michael G., Simpson, David J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8407380/
https://www.ncbi.nlm.nih.gov/pubmed/34402641
http://dx.doi.org/10.1128/mSystems.00378-21
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author Wang, Zhiying
Hu, Huifeng
Zhu, Tongbo
Zheng, Jinshui
Gänzle, Michael G.
Simpson, David J.
author_facet Wang, Zhiying
Hu, Huifeng
Zhu, Tongbo
Zheng, Jinshui
Gänzle, Michael G.
Simpson, David J.
author_sort Wang, Zhiying
collection PubMed
description The transmissible locus of stress tolerance (tLST) is a genomic island which confers resistance to heat and chlorine. In this study, we determined that the tLST is frequent in genomes of those Enterobacteriaceae that occur in association with plants as well as the intestines of humans and animals and are relevant as nosocomial pathogens, e.g., Klebsiella and Cronobacter species. The tLST is more frequent in environmental and clinical isolates of Klebsiella pneumoniae than in animal isolates, and heat and chlorine resistance of tLST-positive strains of K. pneumoniae matched the resistance of tLST-positive strains of Escherichia coli. The function of 13 tLST genes was determined by assessing the heat and chlorine resistance of E. coli MG1655 mutants. The deletion of sHsp20, clpK(GI), sHsp(GI), pscA, pscB, and hdeD(GI) reduced both heat and chlorine resistance; deletion of kefB reduced only chlorine resistance. Genes coding for heat shock proteins sHsp20, clpK(GI), and sHsp(GI) decreased the oxidation of cytoplasmic proteins, while kefB decreased the oxidation of membrane lipids. The fitness cost of the tLST for E. coli MG1655 was assessed by pairwise competition experiments with isogenic tLST-positive or tLST-negative strains. The tLST imposes a fitness cost that is compensated for by frequent and lethal challenges with chlorine. All core genes need to be present to maintain the ecological advantage relative to the fitness cost. Taken together, core tLST genes are necessary to provide protection for E. coli against heat and chlorine stress, and the selective pressure for the tLST maintains core genes. IMPORTANCE The transmissible locus of stress tolerance (tLST) is a genomic island comprising 10 core genes that occurs in diverse Enterobacteriaceae and confers resistance to heat and chlorine. Experimentation described in the manuscript describes the physiological function of the core genes by characterization of the resistance of 13 single-knockout (KO) mutants and by characterization of protein and membrane oxidation in these strains after chlorine challenge. Results identify tLST resistance as a genomic island that is specific for those Enterobacteriaceae that occur in plant-associated habitats as well in the intestines of vertebrates. In addition, the ecological function of the genomic island was characterized by large-scale genomic analysis and competition experiments of wild-type and mutant strains. Results suggest that tLST-mediated resistance to chlorine may contribute to the persistence of nosocomial pathogens in hospitals.
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spelling pubmed-84073802021-09-09 Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae Wang, Zhiying Hu, Huifeng Zhu, Tongbo Zheng, Jinshui Gänzle, Michael G. Simpson, David J. mSystems Research Article The transmissible locus of stress tolerance (tLST) is a genomic island which confers resistance to heat and chlorine. In this study, we determined that the tLST is frequent in genomes of those Enterobacteriaceae that occur in association with plants as well as the intestines of humans and animals and are relevant as nosocomial pathogens, e.g., Klebsiella and Cronobacter species. The tLST is more frequent in environmental and clinical isolates of Klebsiella pneumoniae than in animal isolates, and heat and chlorine resistance of tLST-positive strains of K. pneumoniae matched the resistance of tLST-positive strains of Escherichia coli. The function of 13 tLST genes was determined by assessing the heat and chlorine resistance of E. coli MG1655 mutants. The deletion of sHsp20, clpK(GI), sHsp(GI), pscA, pscB, and hdeD(GI) reduced both heat and chlorine resistance; deletion of kefB reduced only chlorine resistance. Genes coding for heat shock proteins sHsp20, clpK(GI), and sHsp(GI) decreased the oxidation of cytoplasmic proteins, while kefB decreased the oxidation of membrane lipids. The fitness cost of the tLST for E. coli MG1655 was assessed by pairwise competition experiments with isogenic tLST-positive or tLST-negative strains. The tLST imposes a fitness cost that is compensated for by frequent and lethal challenges with chlorine. All core genes need to be present to maintain the ecological advantage relative to the fitness cost. Taken together, core tLST genes are necessary to provide protection for E. coli against heat and chlorine stress, and the selective pressure for the tLST maintains core genes. IMPORTANCE The transmissible locus of stress tolerance (tLST) is a genomic island comprising 10 core genes that occurs in diverse Enterobacteriaceae and confers resistance to heat and chlorine. Experimentation described in the manuscript describes the physiological function of the core genes by characterization of the resistance of 13 single-knockout (KO) mutants and by characterization of protein and membrane oxidation in these strains after chlorine challenge. Results identify tLST resistance as a genomic island that is specific for those Enterobacteriaceae that occur in plant-associated habitats as well in the intestines of vertebrates. In addition, the ecological function of the genomic island was characterized by large-scale genomic analysis and competition experiments of wild-type and mutant strains. Results suggest that tLST-mediated resistance to chlorine may contribute to the persistence of nosocomial pathogens in hospitals. American Society for Microbiology 2021-08-17 /pmc/articles/PMC8407380/ /pubmed/34402641 http://dx.doi.org/10.1128/mSystems.00378-21 Text en Copyright © 2021 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wang, Zhiying
Hu, Huifeng
Zhu, Tongbo
Zheng, Jinshui
Gänzle, Michael G.
Simpson, David J.
Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae
title Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae
title_full Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae
title_fullStr Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae
title_full_unstemmed Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae
title_short Ecology and Function of the Transmissible Locus of Stress Tolerance in Escherichia coli and Plant-Associated Enterobacteriaceae
title_sort ecology and function of the transmissible locus of stress tolerance in escherichia coli and plant-associated enterobacteriaceae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8407380/
https://www.ncbi.nlm.nih.gov/pubmed/34402641
http://dx.doi.org/10.1128/mSystems.00378-21
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