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Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity
BACKGROUND: Bacteria produce small molecule iron chelators, known as siderophores, to facilitate the acquisition of iron from the environment. The synthesis of more than one siderophore and the production of multiple siderophore uptake systems by a single bacterial species are common place. The sele...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2012
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3465284/ https://www.ncbi.nlm.nih.gov/pubmed/23071628 http://dx.doi.org/10.1371/journal.pone.0046754 |
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author | Adler, Conrado Corbalán, Natalia S. Seyedsayamdost, Mohammad R. Pomares, María Fernanda de Cristóbal, Ricardo E. Clardy, Jon Kolter, Roberto Vincent, Paula A. |
author_facet | Adler, Conrado Corbalán, Natalia S. Seyedsayamdost, Mohammad R. Pomares, María Fernanda de Cristóbal, Ricardo E. Clardy, Jon Kolter, Roberto Vincent, Paula A. |
author_sort | Adler, Conrado |
collection | PubMed |
description | BACKGROUND: Bacteria produce small molecule iron chelators, known as siderophores, to facilitate the acquisition of iron from the environment. The synthesis of more than one siderophore and the production of multiple siderophore uptake systems by a single bacterial species are common place. The selective advantages conferred by the multiplicity of siderophore synthesis remains poorly understood. However, there is growing evidence suggesting that siderophores may have other physiological roles besides their involvement in iron acquisition. METHODS AND PRINCIPAL FINDINGS: Here we provide the first report that pyochelin displays antibiotic activity against some bacterial strains. Observation of differential sensitivity to pyochelin against a panel of bacteria provided the first indications that catecholate siderophores, produced by some bacteria, may have roles other than iron acquisition. A pattern emerged where only those strains able to make catecholate-type siderophores were resistant to pyochelin. We were able to associate pyochelin resistance to catecholate production by showing that pyochelin-resistant Escherichia coli became sensitive when biosynthesis of its catecholate siderophore enterobactin was impaired. As expected, supplementation with enterobactin conferred pyochelin resistance to the entE mutant. We observed that pyochelin-induced growth inhibition was independent of iron availability and was prevented by addition of the reducing agent ascorbic acid or by anaerobic incubation. Addition of pyochelin to E. coli increased the levels of reactive oxygen species (ROS) while addition of ascorbic acid or enterobactin reduced them. In contrast, addition of the carboxylate-type siderophore, citrate, did not prevent pyochelin-induced ROS increases and their associated toxicity. CONCLUSIONS: We have shown that the catecholate siderophore enterobactin protects E. coli against the toxic effects of pyochelin by reducing ROS. Thus, it appears that catecholate siderophores can behave as protectors of oxidative stress. These results support the idea that siderophores can have physiological roles aside from those in iron acquisition. |
format | Online Article Text |
id | pubmed-3465284 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-34652842012-10-15 Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity Adler, Conrado Corbalán, Natalia S. Seyedsayamdost, Mohammad R. Pomares, María Fernanda de Cristóbal, Ricardo E. Clardy, Jon Kolter, Roberto Vincent, Paula A. PLoS One Research Article BACKGROUND: Bacteria produce small molecule iron chelators, known as siderophores, to facilitate the acquisition of iron from the environment. The synthesis of more than one siderophore and the production of multiple siderophore uptake systems by a single bacterial species are common place. The selective advantages conferred by the multiplicity of siderophore synthesis remains poorly understood. However, there is growing evidence suggesting that siderophores may have other physiological roles besides their involvement in iron acquisition. METHODS AND PRINCIPAL FINDINGS: Here we provide the first report that pyochelin displays antibiotic activity against some bacterial strains. Observation of differential sensitivity to pyochelin against a panel of bacteria provided the first indications that catecholate siderophores, produced by some bacteria, may have roles other than iron acquisition. A pattern emerged where only those strains able to make catecholate-type siderophores were resistant to pyochelin. We were able to associate pyochelin resistance to catecholate production by showing that pyochelin-resistant Escherichia coli became sensitive when biosynthesis of its catecholate siderophore enterobactin was impaired. As expected, supplementation with enterobactin conferred pyochelin resistance to the entE mutant. We observed that pyochelin-induced growth inhibition was independent of iron availability and was prevented by addition of the reducing agent ascorbic acid or by anaerobic incubation. Addition of pyochelin to E. coli increased the levels of reactive oxygen species (ROS) while addition of ascorbic acid or enterobactin reduced them. In contrast, addition of the carboxylate-type siderophore, citrate, did not prevent pyochelin-induced ROS increases and their associated toxicity. CONCLUSIONS: We have shown that the catecholate siderophore enterobactin protects E. coli against the toxic effects of pyochelin by reducing ROS. Thus, it appears that catecholate siderophores can behave as protectors of oxidative stress. These results support the idea that siderophores can have physiological roles aside from those in iron acquisition. Public Library of Science 2012-10-05 /pmc/articles/PMC3465284/ /pubmed/23071628 http://dx.doi.org/10.1371/journal.pone.0046754 Text en © 2012 Adler et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Adler, Conrado Corbalán, Natalia S. Seyedsayamdost, Mohammad R. Pomares, María Fernanda de Cristóbal, Ricardo E. Clardy, Jon Kolter, Roberto Vincent, Paula A. Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity |
title | Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity |
title_full | Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity |
title_fullStr | Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity |
title_full_unstemmed | Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity |
title_short | Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity |
title_sort | catecholate siderophores protect bacteria from pyochelin toxicity |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3465284/ https://www.ncbi.nlm.nih.gov/pubmed/23071628 http://dx.doi.org/10.1371/journal.pone.0046754 |
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