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The role of FoxA, FiuA, and FpvB in iron acquisition via hydroxamate-type siderophores in Pseudomonas aeruginosa

ABSTRACT: Siderophores are specialized molecules with different chemical structures, produced by bacteria and fungi to scavenge iron from the environment, a crucial nutrient for their growth and metabolism. These iron-chelating compounds enable bacteria to overcome iron limitation, a key factor in microbial survival and pathogenesis. Catecholate-type siderophores are primarily produced by bacteria, while hydroxamates are predominantly produced by fungi. The capacity of nine hydroxamate-type siderophores produced by fungi to serve as siderophores for iron acquisition by Pseudomonas aeruginosa, a human pathogen, has been investigated. Growth assays under iron limitation and 55Fe incorporation tests clearly highlighted that all nine siderophores promoted bacterial growth and facilitated iron transport. Additionally, the study aimed to identify the TonB-dependent transporters (TBDTs) responsible for iron import mediated by the tested siderophores. Mutant strains lacking genes encoding TBDTs were employed, revealing that iron is imported into P. aeruginosa cells solely by FpvB for the siderophores coprogen, triacetylfusarinine C, fusigen, ferrirhodin, and ferrirubin siderophores. Iron complexed by desferioxamine G is imported by two TBDTs, FpvB and FoxA. Ferricrocin-Fe and ferrichrycin-Fe complexes are imported by FpvB and FiuA. Lastly, rhodotorulic acid-Fe complexes are imported by FpvB, FiuA, and another unidentified TBDT. In conclusion, the data illustrate the effectiveness of hydroxamate-type siderophores in transporting iron into P. aeruginosa cells and provide insights into the intricate molecular mechanisms involved in iron acquisition, which have implications for understanding bacterial pathogenesis and developing potential therapeutic strategies.

INSTRUMENT(S): timsTOF Pro 2, Q Exactive

ORGANISM(S): Pseudomonas Aeruginosa Pao1

SUBMITTER: Johana Chicher

LAB HEAD: Isabelle J.

PROVIDER: PXD052483 | Pride | 2024-08-26

REPOSITORIES: Pride

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			Action	DRS
	2019_S46_VNormant_13_FCR-1_500ng.mgf	Mgf
	2019_S46_VNormant_13_FCR-1_500ng.raw	Raw
	2019_S46_VNormant_14_FCR-2_500ng.mgf	Mgf
	2019_S46_VNormant_14_FCR-2_500ng.raw	Raw
	2019_S46_VNormant_15_FCR-3_500ng.mgf	Mgf

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Project description:High-affinity iron (Fe) scavenging compounds, or siderophores, are widely employed by soil bacteria to survive scarcity in bioavailable Fe. Siderophore biosynthesis relies on cellular carbon metabolism, despite reported decrease in both carbon uptake and Fe-containing metabolic proteins in Fe-deficient cells. Given this paradox, the metabolic network required to sustain the Fe-scavenging strategy is poorly understood. Here, through multiple 13C-metabolomics experiments with Fe-replete and Fe-limited cells, we uncover how soil Pseudomonas species reprogram their metabolic pathways to prioritize siderophore biosynthesis. Across the three species investigated (Pseudomonas putida KT2440, Pseudomonas protegens Pf-5, and Pseudomonas putida S12), siderophore secretion is higher during growth on gluconeogenic substrates than during growth on glycolytic substrates. In response to Fe limitation, we capture decreased flux toward the tricarboxylic acid (TCA) cycle during the metabolism of glycolytic substrates but, due to carbon recycling to the TCA cycle via enhanced anaplerosis, the metabolism of gluconeogenic substrates results in an increase in both siderophore secretion (up to threefold) and Fe extraction (up to sixfold) from soil minerals. During simultaneous feeding on the different substrate types, Fe deficiency triggers a hierarchy in substrate utilization, which is facilitated by changes in protein abundances for substrate uptake and initial catabolism. Rerouted metabolism further promotes favorable fluxes in the TCA cycle and the gluconeogenesis-anaplerosis nodes, despite decrease in several proteins in these pathways, to meet carbon and energy demands for siderophore precursors in accordance with increased proteins for siderophore biosynthesis. Hierarchical carbon metabolism thus serves as a critical survival strategy during the metal nutrient deficiency. Data availability:The proteomics data have been deposited into the ProteomeXchange Consortium via the PRIDE partner repository with the data set identifier <a href='https://www.ebi.ac.uk/pride/archive/projects/PXD013605' rel='noopener noreferrer' target='_blank'>PXD013605</a>.

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The role of FoxA, FiuA, and FpvB in iron acquisition via hydroxamate-type siderophores in Pseudomonas aeruginosa

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