Stephan M. Kraemer

Iron oxide dissolution and solubility in the presence of siderophores

Abstract.Iron is an essential trace nutrient for most known organisms. The iron availability is limited by the solubility and the slow dissolution kinetics of iron-bearing mineral phases, particularly in pH neutral or alkaline environments such as carbonatic soils and ocean water. Bacteria, fungi, and plants have evolved iron acquisition systems to increase the bioavailability of iron in such environments. A particularly efficient iron acquisition system involves the solubilization of iron by siderophores. Siderophores are biogenic chelators with high affinity and specificity for iron complexation.This review focuses on the geochemical aspects of biological iron acquisition. The significance of iron-bearing minerals as nutrient source for siderophore-promoted iron acquisition has been confirmed in microbial culture studies. Due to the extraordinary thermodynamic stability of soluble siderophore-iron complexes, siderophores have a pronounced effect on the solubility of iron oxides over a wide pH range. Very small concentrations of free siderophores in solution have a large effect on the solution saturation state of iron oxides. This siderophore induced disequilibrium can drive dissolution mechanisms such as proton-promoted or ligand-promoted iron oxide dissolution. The adsorption of siderophores to oxide surfaces also induces a direct siderophore-promoted surface-controlled dissolution mechanism. The efficiency of siderophores for increasing the solubility and dissolution kinetics of iron oxides are compared to other natural and anthropogenic ligands.

Steady-state dissolution kinetics of goethite in the presence of desferrioxamine B and oxalate ligands: implications for the microbial acquisition of iron

This paper reports an investigation of the effects of a trihydroxamate siderophore, desferrioxamine B (DFO-B), and a common biological ligand, oxalate, on the steady-state dissolution of goethite at pH 5 and 25 °C. The main goal of our study was to quantify the adsorption of the ligands and the dissolution of goethite they promote in a two-ligand system. In systems with one ligand only, the adsorption of oxalate and DFO-B each followed an L-type isotherm. The surface excess of oxalate was approximately 40 mmol kg−1 at solution concentrations above 80 μM, whereas the surface excess of DFO-B was only 1.2 mmol kg−1 at 80 μM solution concentration. In the two-ligand systems, oxalate decreased DFO-B adsorption quite significantly, but not vice versa. For example, in solutions containing 40 μM DFO-B and 40 μM oxalate, 30% of the DFO-B adsorbed in the absence of oxalate was displaced. The mass-normalized dissolution rate of goethite in the presence of DFO-B alone increased as the surface excess of the ligand increased, suggesting a ligand-promoted dissolution mechanism. In systems containing oxalate only, mass-normalized goethite dissolution rates were very low at concentrations below 200 μM, despite maximal adsorption of the ligand. At higher oxalate concentrations (up to 8 mM), the steady-state dissolution rate continued to increase, even though the surface excess of adsorbed ligand was essentially constant. Chemical affinity calculations and dissolution experiments with variation of the reactor flow rate showed that far-from-equilibrium conditions did not obtain in systems containing oxalate at concentrations below 5 mM. The dissolution rate in the presence of DFO-B at solution concentrations between 1 and 80 μM was approximately doubled when oxalate was also present at 40 μM solution concentration. The dissolution rate in the presence of oxalate at solution concentrations between 0 and 200 μM was increased by more than an order of magnitude when DFO-B was also present at 40 μM solution concentration. Chemical affinity calculations showed that, in systems containing DFO-B, goethite dissolution was always under far-from-equilibrium conditions, irrespective of the presence of oxalate. These results were described quantitatively by a model rate law containing a term proportional to the surface excess of DFO-B and a term proportional to that of oxalate, with both surface excesses being determined in the two-ligand system. The pseudo first-order rate coefficient in the DFO-B term has the same value as measured for goethite dissolution in the presence of DFO-B only, while the rate coefficient in the oxalate term must be measured in the two-ligand system, since it is only in this system that far-from-equilibrium conditions obtain. These latter conditions do not exist in the system containing oxalate only, but they do exist in the DFO-B/oxalate system because the siderophore is able to remove Fe(III) from all Fe–oxalate complexes rapidly, leaving the uncomplexed oxalate ligand in solution free to react again with the goethite surface. This synergy observed in the two-ligand system implies that the production of modest quantities of siderophore in the presence of very low concentrations of oxalate would be an extremely effective mechanism for the microbially induced release of Fe from goethite.

Effect of hydroxamate siderophores on Fe release and Pb(II) adsorption by goethite

Abstract Hydroxamate siderophores are biologically-synthesized, Fe(III)-specific ligands which are common in soil environments. In this paper, we report an investigation of their adsorption by the iron oxyhydroxide, goethite; their influence on goethite dissolution kinetics; and their ability to affect Pb(II) adsorption by the goethite surface. The siderophores used were desferrioxamine B (DFO-B), a fungal siderophore, and desferrioxamine D1, an acetyl derivative of DFO-B (DFO-D1). Siderophore adsorption isotherms yielded maximum surface concentrations of 1.5 (DFO-B) or 3.5 (DFO-D1) μmol/g at pH 6.6, whereas adsorption envelopes showed either cation-like (DFO-B) or ligand-like (DFO-D1) behavior. Above pH 8, the adsorbed concentrations of both siderophores were similar. The dissolution rate of goethite in the presence of 240 μM DFO-B or DFO-D1 was 0.02 or 0.17 μmol/g hr, respectively. Comparison of these results with related literature data on the reactions between goethite and acetohydroxamic acid, a monohydroxamate ligand, suggested that the three hydroxamate groups in DFO-D1 coordinate to Fe(III) surface sites relatively independently. The results also demonstrated a significant depleting effect of 240 μM DFO-B or DFO-D1 on Pb(II) adsorption by goethite at pH > 6.5, but there was no effect of adsorbed Pb(II) on the goethite dissolution rate.

Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes

Iron is an essential element for plants and microbes. However, in most cultivated soils, the concentration of iron available for these living organisms is very low because its solubility is controlled by stable hydroxides, oxyhydroxides and oxides. In the rhizosphere, there is a high demand of iron because of the iron uptake by plants, and microorganisms which density and activity are promoted by the release of root exudates. Plants and microbes have evolved active strategies of iron uptake. Iron incorporation by these organisms lead to complex interactions ranging from competition to mutualism. These complex interactions are under the control of physico-chemical properties of the soils in which they occur, and reciprocally iron uptake strategies of plants and microbes impact these soil properties. These iron-mediated interactions between soils, plants and microbes impact the plant growth and health and their analysis, together with that of the resulting iron dynamics, is of a major agronomic interest. Analysis of the complex interactions soils, plants and microbes represent also a unique opportunity to progress in our knowledge of the rhizosphere ecology. This progression requires merging complementary expertises and study strategies in soil science, plant biology and microbiology. This review provides information on (i) iron status in soil and rhizosphere, iron uptake by plants and microbes, and on (ii) the corresponding study strategies. Finally, illustrations of how integration of these approaches allows gaining knowledge in the complex interactions occurring in the rhizosphere are given.

Goethite dissolution in the presence of phytosiderophores : rates, mechanisms, and the synergistic effect of oxalate

The purpose of this study was the elucidation of the chemical mechanism of an important process in iron acquisition by graminaceous plants: the dissolution of iron oxides in the presence of phytosiderophores. We were particularly interested in the effects of diurnal root exudation of phytosiderophores and of the presence of other organic ligands in the rhizosphere of graminaceous plants on the dissolution mechanism.Phytosiderophores of the type 2′-deoxymugineic acid (DMA) were purified from the root exudates of wheat plants (Triticum aestivum L. cv. Tamaro). DMA-promoted dissolution of goethite under steady-state and non-steady-state conditions and its dependence on pH, adsorbed DMA concentration, and the presence of the organic ligand oxalate were studied. We show that dissolution of goethite by phytosiderophores follows a surface controlled ligand promoted dissolution mechanism. We also found that oxalate, an organic ligand commonly found in rhizosphere soils, has a synergistic effect on the steady-state dissolution of goethite by DMA. Under non-steady-state addition of the phytosiderophore, mimicking the diurnal exudation pattern of phytosiderophore release, a fast dissolution of iron is triggered in the presence of oxalate.To investigate the efficiency of these mechanisms in plant iron acquisition, wheat plants were grown on a substrate amended with goethite as only iron source. The chlorophyll status of these plants was similar to iron-fertilized plants and significantly higher than in plants grown in iron free nutrient solutions. This demonstrates that wheat can efficiently mobilize iron, even from well crystalline goethite that is usually considered unavailable for plant nutrition.

Temperature dependence of goethite dissolution promoted by trihydroxamate siderophores

This article reports an investigation of the temperature dependence of goethite dissolution kinetics in the presence of desferrioxamine B (DFO-B), a trihydroxamate siderophore, and its acetyl derivative, desferrioxamine D1 (DFO-D1). At 25 and 40°C, DFO-D1 dissolved goethite at twice the rate of DFO-B, whereas at 55°C, the behavior of the two ligands was almost the same. Increasing the temperature from 25 to 55°C caused little or no significant change in DFO-B or DFO-D1 adsorption by goethite. A pseudo-first-order rate coefficient for dissolution, calculated as the ratio of the mass-normalized dissolution rate coefficient to the surface excess of siderophore, was approximately the same at 25 and 40°C for both siderophores. At 55°C, however, this rate coefficient for DFO-D1 was about half that for DFO-B. Analysis of the temperature dependence of the mass-normalized dissolution rate coefficient via the Arrhenius equation led to an apparent activation energy that was larger for DFO-B than for DFO-D1, but much smaller than that reported for the proton-promoted dissolution of goethite. A compensation law was found to relate the pre-exponential factor to the apparent activation energy in the Arrhenius equation, in agreement with what has been noted for the proton-promoted dissolution of oxide minerals and for the complexation of Fe3+ by DFO-B and simple hydroxamate ligands in aqueous solution. Analysis of these results suggested that the siderophores adsorb on goethite with a only single hydroxamate group in bidentate ligation with an Fe(III) center.

Geochemical Aspects of Phytosiderophore‐Promoted Iron Acquisition by Plants

Iron is an essential trace nutrient for all plants. The acquisition of iron is limited by low solubilities and slow dissolution rates of iron‐bearing minerals in many soils. Therefore, iron limitation can be an important nutritional disorder in crop plants, leading to decreased yields or significant costs for iron fertilization. However, some species among the group of graminaceous plants (including wheat and barley) exhibit a rather low susceptibility to iron deficiency. These species respond to iron‐limiting conditions by the exudation of ligands with a high affinity and specificity for iron complexation, the so‐called phytosiderophores. Soluble iron–phytosiderophore complexes are recognized and transported across the root plasma membrane by specific transport proteins. This chapter focuses on geochemical aspects of this so‐called “strategy II” iron acquisition mechanism. The coordination chemistry of phytosiderophores and their iron complexes in the soil solution are discussed and compared to other organic ligands including low‐molecular weight organic acids and microbial siderophores. The properties of iron complexes and iron‐bearing minerals in the rhizosphere are discussed and compared with regard to their potential as sources of plant available iron. An important focus of this chapter is the elucidation of the thermodynamics, mechanisms, and rates of iron acquisition from these sources by phytosiderophores. Thus, we hope to contribute to the understanding of iron acquisition by strategy II plants in particular and of iron cycling in the rhizosphere in general.

Iron isotope fractionation during Fe uptake and translocation in alpine plants.

The potential of stable Fe isotopes as a tracer for the biogeochemical Fe cycle depends on the understanding and quantification of the fractionation processes involved. Iron uptake and cycling by plants may influence Fe speciation in soils. Here, we determined the Fe isotopic composition of different plant parts including the complete root system of three alpine plant species (Oxyria digyna, Rumex scutatus, Agrostis gigantea) in a granitic glacier forefield, which allowed us, for the first time, to distinguish between uptake and in-plant fractionation processes. The overall range of fractionation was 4.5 per thousand in delta(56)Fe. Mass balance calculations demonstrated that fractionation toward lighter Fe isotopic composition occurred in two steps during uptake: (1) before active uptake, probably during mineral dissolution and (2) during selective uptake of Fe at the plasma membrane with an enrichment factor of -1.0 to -1.7 per thousand for all three species. Iron isotopes were further fractionated during remobilization from old into new plant tissue, which changed the isotopic composition of leaves and flowers over the season. This study demonstrates the potential of Fe isotopes as a new tool in plant nutrition studies but also reveals challenges for the future application of Fe isotope signatures in soil-plant environments.

Root exudation of phytosiderophores from soil‐grown wheat

For the first time, phytosiderophore (PS) release of wheat (Triticum aestivum cv Tamaro) grown on a calcareous soil was repeatedly and nondestructively sampled using rhizoboxes combined with a recently developed root exudate collecting tool. As in nutrient solution culture, we observed a distinct diurnal release rhythm; however, the measured PS efflux was c. 50 times lower than PS exudation from the same cultivar grown in zero iron (Fe)-hydroponic culture. Phytosiderophore rhizosphere soil solution concentrations and PS release of the Tamaro cultivar were soil-dependent, suggesting complex interactions of soil characteristics (salinity, trace metal availability) and the physiological status of the plant and the related regulation (amount and timing) of PS release. Our results demonstrate that carbon and energy investment into Fe acquisition under natural growth conditions is significantly smaller than previously derived from zero Fe-hydroponic studies. Based on experimental data, we calculated that during the investigated period (21–47 d after germination), PS release initially exceeded Fe plant uptake 10-fold, but significantly declined after c. 5 wk after germination. Phytosiderophore exudation observed under natural growth conditions is a prerequisite for a more accurate and realistic assessment of Fe mobilization processes in the rhizosphere using both experimental and modeling approaches.

The influence of pH on iron speciation in podzol extracts: Iron complexes with natural organic matter, and iron mineral nanoparticles

The quantities of natural organic matter (NOM) and associated iron (Fe) in soil extracts are known to increase with increasing extractant pH. However, it was unclear how the extraction pH affects Fe speciation for particles below 30 nm. We used flow field-flow fractionation (FlowFFF) and transmission electron microscopy (TEM) to investigate the association of Fe and trace elements with NOM and nanoparticulate iron (oxy)hydroxides in podzol extracts. For extracts prepared at the native soil pH (~4), and within a 1-30 nm size range, Fe was associated with NOM. In extracts with a pH≥7 from the E and B soil horizons, Fe was associated with NOM as well as with iron (oxy)hydroxide nanoparticles with a size of approximately 10 nm. The iron (oxy)hydroxide nanoparticles may have either formed within the soil extracts in response to the increase in pH, or they were mobilized from the soil. Additionally, pH shift experiments showed that iron (oxy)hydroxides formed when the native soil pH (~4) was increased to 9 following the extraction. The iron (oxy)hydroxide nanoparticles aggregated if the pH was decreased from 9 to 4. The speciation of Fe also influenced trace element speciation: lead was partly associated with the iron (oxy)hydroxides (when present), while copper binding to NOM remained unaffected by the presence of iron (oxy)hydroxide nanoparticles. The results of this study are important for interpreting the representativeness of soil extracts prepared at a pH other than the native soil pH, and for understanding the changes in Fe speciation that occur along a pH gradient.