Beyond iron: the role of siderophores in the biogeochemistry of late first-row transition metals

Abstract

Siderophores are a group of organic ligands released by bacteria, fungi, and grasses with a high affinity for Fe3+; they are found ubiquitously in natural solutions. Organisms primarily secrete siderophores to overcome the limitations of low iron bioavailability. However, there is strong evidence that siderophores play a wider role in the cycling of trace metals. To that end, the aim of this thesis is to improve our understanding of metal-siderophore chemistry and the role of siderophores in the acquisition and uptake of micronutrients in the environment beyond iron, with a special focus on the rhizosphere. First, density functional theory (DFT) is used to study the structure, stability, and bonding of late first-row transition metal-deoxymugineic acid (M-DMA) complexes. DMA is a plant-produced siderophore (phytosiderophore), which has previously been implicated in the zinc efficiency of rice. Based on the geometry of the low-energy M-DMA conformers, modifications are suggested for the structure of DMA to adapt the ligand from a siderophore into a zincophore. A strong correlation between ligand-to-metal charge transfer and experimental stability constants is evidenced for M-DMA complexes. Next, a combination of potentiometric titrations and geochemical speciation modelling are used to determine the pH and ionic strength ligand interchange points (LIPs) for the exchange of zinc between citrate and DFOB. The calculated LIPs fall within the pH and ionic strength gradients expected in the rice rhizosphere. This suggests that cooperative weak/strong ligand interactions play a role in zinc uptake by rice. The same methodological approach is used to quantify the effect of salinity on the zinc binding efficiency of siderophore functional groups. The order of increasing susceptibility of siderophore classes to salinity in terms of their zinc chelating ability is: hydroxamate < catecholate < α-hydroxycarboxylate. Since α-hydroxycarboxylate ligands are associated with phytosiderophores, plant productivity is predicted to be more sensitive to salinization than either bacterial or fungal productivity. Finally, tools are developed for fingerprinting metal-siderophore complexes in the environment. The uncertainty in theoretical calculations of isotopic signatures is quantified and an updated DFT protocol is proposed for calculating accurate metal stable isotope signatures.