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Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions

Siderophores are soluble or membrane-embedded molecules that bind the oxidized form of iron, Fe(III), and play roles in iron acquisition by microorganisms. Fe(III)-bound siderophores bind to specific receptors that allow microbes to acquire iron. However, certain soil microbes release a compound (pu...

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Autores principales: Charron-Lamoureux, Vincent, Haroune, Lounès, Pomerleau, Maude, Hall, Léo, Orban, Frédéric, Leroux, Julie, Rizzi, Adrien, Bourassa, Jean-Sébastien, Fontaine, Nicolas, d’Astous, Élodie V., Dauphin-Ducharme, Philippe, Legault, Claude Y., Bellenger, Jean-Philippe, Beauregard, Pascale B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10156857/
https://www.ncbi.nlm.nih.gov/pubmed/37137890
http://dx.doi.org/10.1038/s41467-023-38222-0
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author Charron-Lamoureux, Vincent
Haroune, Lounès
Pomerleau, Maude
Hall, Léo
Orban, Frédéric
Leroux, Julie
Rizzi, Adrien
Bourassa, Jean-Sébastien
Fontaine, Nicolas
d’Astous, Élodie V.
Dauphin-Ducharme, Philippe
Legault, Claude Y.
Bellenger, Jean-Philippe
Beauregard, Pascale B.
author_facet Charron-Lamoureux, Vincent
Haroune, Lounès
Pomerleau, Maude
Hall, Léo
Orban, Frédéric
Leroux, Julie
Rizzi, Adrien
Bourassa, Jean-Sébastien
Fontaine, Nicolas
d’Astous, Élodie V.
Dauphin-Ducharme, Philippe
Legault, Claude Y.
Bellenger, Jean-Philippe
Beauregard, Pascale B.
author_sort Charron-Lamoureux, Vincent
collection PubMed
description Siderophores are soluble or membrane-embedded molecules that bind the oxidized form of iron, Fe(III), and play roles in iron acquisition by microorganisms. Fe(III)-bound siderophores bind to specific receptors that allow microbes to acquire iron. However, certain soil microbes release a compound (pulcherriminic acid, PA) that, upon binding to Fe(III), forms a precipitate (pulcherrimin) that apparently functions by reducing iron availability rather than contributing to iron acquisition. Here, we use Bacillus subtilis (PA producer) and Pseudomonas protegens as a competition model to show that PA is involved in a peculiar iron-managing system. The presence of the competitor induces PA production, leading to precipitation of Fe(III) as pulcherrimin, which prevents oxidative stress in B. subtilis by restricting the Fenton reaction and deleterious ROS formation. In addition, B. subtilis uses its known siderophore bacillibactin to retrieve Fe(III) from pulcherrimin. Our findings indicate that PA plays multiple roles by modulating iron availability and conferring protection against oxidative stress during inter-species competition.
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spelling pubmed-101568572023-05-05 Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions Charron-Lamoureux, Vincent Haroune, Lounès Pomerleau, Maude Hall, Léo Orban, Frédéric Leroux, Julie Rizzi, Adrien Bourassa, Jean-Sébastien Fontaine, Nicolas d’Astous, Élodie V. Dauphin-Ducharme, Philippe Legault, Claude Y. Bellenger, Jean-Philippe Beauregard, Pascale B. Nat Commun Article Siderophores are soluble or membrane-embedded molecules that bind the oxidized form of iron, Fe(III), and play roles in iron acquisition by microorganisms. Fe(III)-bound siderophores bind to specific receptors that allow microbes to acquire iron. However, certain soil microbes release a compound (pulcherriminic acid, PA) that, upon binding to Fe(III), forms a precipitate (pulcherrimin) that apparently functions by reducing iron availability rather than contributing to iron acquisition. Here, we use Bacillus subtilis (PA producer) and Pseudomonas protegens as a competition model to show that PA is involved in a peculiar iron-managing system. The presence of the competitor induces PA production, leading to precipitation of Fe(III) as pulcherrimin, which prevents oxidative stress in B. subtilis by restricting the Fenton reaction and deleterious ROS formation. In addition, B. subtilis uses its known siderophore bacillibactin to retrieve Fe(III) from pulcherrimin. Our findings indicate that PA plays multiple roles by modulating iron availability and conferring protection against oxidative stress during inter-species competition. Nature Publishing Group UK 2023-05-03 /pmc/articles/PMC10156857/ /pubmed/37137890 http://dx.doi.org/10.1038/s41467-023-38222-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Charron-Lamoureux, Vincent
Haroune, Lounès
Pomerleau, Maude
Hall, Léo
Orban, Frédéric
Leroux, Julie
Rizzi, Adrien
Bourassa, Jean-Sébastien
Fontaine, Nicolas
d’Astous, Élodie V.
Dauphin-Ducharme, Philippe
Legault, Claude Y.
Bellenger, Jean-Philippe
Beauregard, Pascale B.
Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
title Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
title_full Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
title_fullStr Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
title_full_unstemmed Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
title_short Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
title_sort pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10156857/
https://www.ncbi.nlm.nih.gov/pubmed/37137890
http://dx.doi.org/10.1038/s41467-023-38222-0
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