Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin

IntroductionGlobisporangium ultimum is an oomycetal pathogen causing damping-off on over 300 different plant hosts. Currently, as for many phytopathogens, its control relies in the use of chemicals with negative impact on health and ecosystems. Therefore, many biocontrol strategies are under investi...

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Main Authors: Camille Grosse, Nathalie Brandt, Pierre Van Antwerpen, René Wintjens, Sandra Matthijs
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1143861/full
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author Camille Grosse
Nathalie Brandt
Pierre Van Antwerpen
René Wintjens
Sandra Matthijs
author_facet Camille Grosse
Nathalie Brandt
Pierre Van Antwerpen
René Wintjens
Sandra Matthijs
author_sort Camille Grosse
collection DOAJ
description IntroductionGlobisporangium ultimum is an oomycetal pathogen causing damping-off on over 300 different plant hosts. Currently, as for many phytopathogens, its control relies in the use of chemicals with negative impact on health and ecosystems. Therefore, many biocontrol strategies are under investigation to reduce the use of fungicides.ResultsIn this study, the soil bacterium Pseudomonas sp. NCIMB 10586 demonstrates a strong iron-repressed in vitro antagonism against G. ultimum MUCL 38045. This antagonism does not depend on the secretion of the broad-range antibiotic mupirocin or of the siderophore pyoverdine by the bacterial strain. The inhibitor molecule was identified as a novel non-ribosomal peptide synthetase (NRPS) siderophore named mupirochelin. Its putative structure bears similarities to other siderophores and bioactive compounds. The transcription of its gene cluster is affected by the biosynthesis of pyoverdine, the major known siderophore of the strain. Besides mupirochelin, we observed the production of a third and novel NRPS-independent siderophore (NIS), here termed triabactin. The iron-responsive transcriptional repression of the two newly identified siderophore gene clusters corroborates their role as iron scavengers. However, their respective contributions to the strain fitness are dissimilar. Bacterial growth in iron-deprived conditions is greatly supported by pyoverdine production and, to a lesser extent, by triabactin. On the contrary, mupirochelin does not contribute to the strain fitness under the studied conditions.ConclusionAltogether, we have demonstrated here that besides pyoverdine, Pseudomonas sp. NCIMB 10586 produces two newly identified siderophores, namely mupirochelin, a weak siderophore with strong antagonism activity against G. ultimum, and the potent siderophore triabactin.
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spelling doaj.art-40dd1ada91ca4e4e83952df183a077742023-03-24T04:36:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-03-011410.3389/fmicb.2023.11438611143861Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactinCamille Grosse0Nathalie Brandt1Pierre Van Antwerpen2René Wintjens3Sandra Matthijs4Unité de Recherche NaturaMonas, Institut de Recherche LABIRIS, Brussels, BelgiumUnité de Recherche NaturaMonas, Institut de Recherche LABIRIS, Brussels, BelgiumRD3 – Pharmacognosy, Bioanalysis and Drug Discovery and Analytical Platform of the Faculty of Pharmacy, Université Libre de Bruxelles, Brussels, BelgiumUnité Microbiologie, Chimie Bioorganique et Macromoléculaire, Department of Research in Drug Development (RD3), Faculty of Pharmacy, Université Libre de Bruxelles, Brussels, BelgiumUnité de Recherche NaturaMonas, Institut de Recherche LABIRIS, Brussels, BelgiumIntroductionGlobisporangium ultimum is an oomycetal pathogen causing damping-off on over 300 different plant hosts. Currently, as for many phytopathogens, its control relies in the use of chemicals with negative impact on health and ecosystems. Therefore, many biocontrol strategies are under investigation to reduce the use of fungicides.ResultsIn this study, the soil bacterium Pseudomonas sp. NCIMB 10586 demonstrates a strong iron-repressed in vitro antagonism against G. ultimum MUCL 38045. This antagonism does not depend on the secretion of the broad-range antibiotic mupirocin or of the siderophore pyoverdine by the bacterial strain. The inhibitor molecule was identified as a novel non-ribosomal peptide synthetase (NRPS) siderophore named mupirochelin. Its putative structure bears similarities to other siderophores and bioactive compounds. The transcription of its gene cluster is affected by the biosynthesis of pyoverdine, the major known siderophore of the strain. Besides mupirochelin, we observed the production of a third and novel NRPS-independent siderophore (NIS), here termed triabactin. The iron-responsive transcriptional repression of the two newly identified siderophore gene clusters corroborates their role as iron scavengers. However, their respective contributions to the strain fitness are dissimilar. Bacterial growth in iron-deprived conditions is greatly supported by pyoverdine production and, to a lesser extent, by triabactin. On the contrary, mupirochelin does not contribute to the strain fitness under the studied conditions.ConclusionAltogether, we have demonstrated here that besides pyoverdine, Pseudomonas sp. NCIMB 10586 produces two newly identified siderophores, namely mupirochelin, a weak siderophore with strong antagonism activity against G. ultimum, and the potent siderophore triabactin.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1143861/fullsiderophorePseudomonasantimicrobialGlobisporangiumgene regulationiron uptake
spellingShingle Camille Grosse
Nathalie Brandt
Pierre Van Antwerpen
René Wintjens
Sandra Matthijs
Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin
Frontiers in Microbiology
siderophore
Pseudomonas
antimicrobial
Globisporangium
gene regulation
iron uptake
title Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin
title_full Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin
title_fullStr Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin
title_full_unstemmed Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin
title_short Two new siderophores produced by Pseudomonas sp. NCIMB 10586: The anti-oomycete non-ribosomal peptide synthetase-dependent mupirochelin and the NRPS-independent triabactin
title_sort two new siderophores produced by pseudomonas sp ncimb 10586 the anti oomycete non ribosomal peptide synthetase dependent mupirochelin and the nrps independent triabactin
topic siderophore
Pseudomonas
antimicrobial
Globisporangium
gene regulation
iron uptake
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1143861/full
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