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

Abstract

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.

Expanding the Pseudomonas diversity of the wheat rhizosphere: four novel species antagonizing fungal phytopathogens and with plant-beneficial properties

“…Finally, a 54 kbp region in the DGS32 genome carries genes very similar to those for the biosynthesis of frederiksenibactin, another siderophore involved in iron acquisition ( Stow et al, 2021 ). NRP-related siderophores in Pseudomonas are known to have antimicrobial activity against fungi and oomycetes ( Buysens et al, 1996 ; Kaplan et al, 2021 ; Grosse et al, 2023 ).…”

SIDERITE: Unveiling Hidden Siderophore Diversity in the Chemical Space Through Digital Exploration

“…Digitalized natural product databases do not offer publicly accessible and searchable instances of "siderophore" and only contain a fraction of currently known siderophores. Previous case-by-case research on siderophores reported their siderophore discoveries by images of the structural formula [10][11][12][13][14] , as do previous reviews and the siderophore base. Although tools are available for converting chemical structure images to SMILES, their accuracy is limited [23][24][25] .…”

“…However, the database was last updated in 2013 and is no longer maintained. Moreover, new siderophore molecules [10][11][12][13] , and even new siderophore ligand types (diazeniumdiolate and 2-nitrosophenol) [14][15][16][17] , are constantly being discovered in various microorganisms. Information regarding these siderophores is currently dispersed across various publications and needs to be systematically recorded.…”

Soil and Mineral Nutrients in Plant Health: A Prospective Study of Iron and Phosphorus in the Growth and Development of Plants

“…In plants that were not infected with the siderophore-producing Pseudomonas strain GRP3 and cultivated in environments with a limited iron supply, the injected plants displayed less chlorotic signs and more chlorophyll [ 169 ]. When nickel is introduced to A. thaliana , the plants were inoculated with two mutants of the Pseudomonas putida ARB86 strain—one overproducing siderophores, and the other lacking siderophore synthesis—the symptoms caused by the metal were relieved to the same degree in plants inoculated with the wild type and both mutants, indicating that siderophore independence is involved, in this case, of alleviating Ni toxicity [ 170 ]. Similarly, two strains of bacteria that produce siderophores decreased the amount of zinc that Salix caprea (willow) absorbed, indicating that siderophores of bacteria may bind to heavy metals in the soil and prevent plants from taking up those metals.…”