Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens

The global rise of antibiotic resistance calls for new drugs against bacterial pathogens. A common approach is to search for natural compounds deployed by microbes to inhibit competitors. Here, we show that the iron-chelating pyoverdines, siderophores produced by environmental Pseudomonas spp., have...

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Main Authors: Vera Vollenweider, Karoline Rehm, Clara Chepkirui, Manuela Pérez-Berlanga, Magdalini Polymenidou, Jörn Piel, Laurent Bigler, Rolf Kümmerli
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/92493
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author Vera Vollenweider
Karoline Rehm
Clara Chepkirui
Manuela Pérez-Berlanga
Magdalini Polymenidou
Jörn Piel
Laurent Bigler
Rolf Kümmerli
author_facet Vera Vollenweider
Karoline Rehm
Clara Chepkirui
Manuela Pérez-Berlanga
Magdalini Polymenidou
Jörn Piel
Laurent Bigler
Rolf Kümmerli
author_sort Vera Vollenweider
collection DOAJ
description The global rise of antibiotic resistance calls for new drugs against bacterial pathogens. A common approach is to search for natural compounds deployed by microbes to inhibit competitors. Here, we show that the iron-chelating pyoverdines, siderophores produced by environmental Pseudomonas spp., have strong antibacterial properties by inducing iron starvation and growth arrest in pathogens. A screen of 320 natural Pseudomonas isolates used against 12 human pathogens uncovered several pyoverdines with particularly high antibacterial properties and distinct chemical characteristics. The most potent pyoverdine effectively reduced growth of the pathogens Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus in a concentration- and iron-dependent manner. Pyoverdine increased survival of infected Galleria mellonella host larvae and showed low toxicity for the host, mammalian cell lines, and erythrocytes. Furthermore, experimental evolution of pathogens combined with whole-genome sequencing revealed limited resistance evolution compared to an antibiotic. Thus, pyoverdines from environmental strains have the potential to become a new class of sustainable antibacterials against specific human pathogens.
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spelling doaj-art-cd4309e4cc2a4a3ab018801568f0dc732025-08-20T02:52:45ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.92493Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogensVera Vollenweider0https://orcid.org/0000-0003-2920-3031Karoline Rehm1Clara Chepkirui2Manuela Pérez-Berlanga3https://orcid.org/0000-0001-9064-9724Magdalini Polymenidou4https://orcid.org/0000-0003-1271-9445Jörn Piel5https://orcid.org/0000-0002-2282-8154Laurent Bigler6https://orcid.org/0000-0003-3548-3594Rolf Kümmerli7https://orcid.org/0000-0003-4084-6679Department of Quantitative Biomedicine, University of Zurich, Zurich, SwitzerlandDepartment of Chemistry, University of Zurich, Zurich, SwitzerlandInstitute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zurich, Zurich, SwitzerlandDepartment of Quantitative Biomedicine, University of Zurich, Zurich, SwitzerlandDepartment of Quantitative Biomedicine, University of Zurich, Zurich, SwitzerlandInstitute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zurich, Zurich, SwitzerlandDepartment of Chemistry, University of Zurich, Zurich, SwitzerlandDepartment of Quantitative Biomedicine, University of Zurich, Zurich, SwitzerlandThe global rise of antibiotic resistance calls for new drugs against bacterial pathogens. A common approach is to search for natural compounds deployed by microbes to inhibit competitors. Here, we show that the iron-chelating pyoverdines, siderophores produced by environmental Pseudomonas spp., have strong antibacterial properties by inducing iron starvation and growth arrest in pathogens. A screen of 320 natural Pseudomonas isolates used against 12 human pathogens uncovered several pyoverdines with particularly high antibacterial properties and distinct chemical characteristics. The most potent pyoverdine effectively reduced growth of the pathogens Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus in a concentration- and iron-dependent manner. Pyoverdine increased survival of infected Galleria mellonella host larvae and showed low toxicity for the host, mammalian cell lines, and erythrocytes. Furthermore, experimental evolution of pathogens combined with whole-genome sequencing revealed limited resistance evolution compared to an antibiotic. Thus, pyoverdines from environmental strains have the potential to become a new class of sustainable antibacterials against specific human pathogens.https://elifesciences.org/articles/92493pyoverdineantibacterial treatmentPseudomonas spp.
spellingShingle Vera Vollenweider
Karoline Rehm
Clara Chepkirui
Manuela Pérez-Berlanga
Magdalini Polymenidou
Jörn Piel
Laurent Bigler
Rolf Kümmerli
Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens
eLife
pyoverdine
antibacterial treatment
Pseudomonas spp.
title Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens
title_full Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens
title_fullStr Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens
title_full_unstemmed Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens
title_short Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens
title_sort antimicrobial activity of iron depriving pyoverdines against human opportunistic pathogens
topic pyoverdine
antibacterial treatment
Pseudomonas spp.
url https://elifesciences.org/articles/92493
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