Siderophore-promoted Dissolution Research Articles

Investigation of Siderophore-Promoted and Reductive Dissolution of Dust in Marine Microenvironments Such as Trichodesmium Colonies

Desert dust is a major source of iron (Fe) to Fe-limited ocean regions. However, Fe-limited phytoplankton often struggle to obtain dust-bound Fe (dust-Fe) due to its low solubility and short residence time in the euphotic zone. Trichodesmium, a globally important nitrogen-fixing, cyanobacterium, is uniquely adapted for utilizing dust as an Fe-source. Trichodesmium can actively collect and concentrate dust particles within the core of its colonies and enhance dust-Fe dissolution rates via two bio-dissolution mechanisms: reduction and complexation by a siderophore. Here, mimicking bio-dissolution in Trichodesmium colonies, we studied the kinetics of desert dust dissolution by a siderophore and a reductant in seawater. By concurrent measurements of dissolved Fe, silica and aluminum we recognized two major mineral pools that released Fe into seawater over an 8-day period: Fe(hydr)oxides and aluminosilicates. In the presence of the siderophore desferrioxamine-B, we observed two stages of dissolution: a short stage of fast Fe dissolution followed by a lasting stage of slow Fe dissolution that was highly correlated to aluminum and silica dissolution. In the presence of the reductant, ascorbate, Fe dissolution was not correlated to aluminum and silica dissolution and was relatively slow. Based on these observations and on dust minerology, we constructed a conceptual model for dust-Fe dissolution by a siderophore and a reductant from two major mineral pools: reductive and siderophore-promoted dissolution of Fe(hydr)oxides and slow continuous dissolution of Fe-bearing clays in the presence of a siderophore. Our findings highlight the importance of clays as an Fe source to Trichodesmium and possibly to marine phytoplankton in general and can be further used to assess the contribution of dust-Fe to the Fe requirements of natural Trichodesmium colonies. From our measured bio-dissolution rates and concentrations of dust retained within colonies from the Gulf of Aqaba, we calculated the supply of dissolved Fe from dust to Trichodesmium. Based on published Fe-quotas and growth rates we calculated Trichodesmium’s Fe requirements under Fe-limited and Fe-replete conditions. The calculated dissolved Fe supply from dust, retained by a colony, can fulfil the minimal Fe requirements of slow growing, Fe-limited colonies, but cannot support fast growth and/or higher cellular Fe quotas.

Siderophore-promoted dissolution of ferrihydrite associated with adsorbed and coprecipitated natural organic matter

Acquisition of Fe(III) from hardly soluble Fe oxyhydroxides by bacteria, fungi and plants in soil is often facilitated by Fe(III)-chelating siderophores. While the siderophore-promoted dissolution of pure Fe oxyhydroxides and the influence of defined low molecular weight organic acids has been investigated meticulously, studies examining Fe oxyhydroxides coated with more complex adsorbed organic matter (OM) or Fe-OM coprecipitates have been sparse. This study therefore explored the impact of the composition of both adsorbed and coprecipitated OM on the siderophore-promoted dissolution of ferrihydrite (Fh) in relation to (i) surface site coverage and pore blockage, (ii)aggregation state, (iii) charge characteristics and (iv) crystallinity. In addition to pure Fh, Fh-OM adsorption complexes and Fe-OM coprecipitates were synthesized using OM of different origins (extracellular polymeric substances of Bacillus subtilis, natural OM (NOM) extracted from soil Oi and Oa horizons). The Fe-organic associations were characterized by N2 gas adsorption, X-ray photoelectron spectroscopy (XPS), electrophoretic mobility, particle size measurements and desorption experiments. Siderophore-mediated dissolution experiments with desferrioxamine-B (DFOB) were conducted at pH 4 and 7. At pH 4, adsorbed OM provided a more effective protection against DFOB due to its larger sorption affinity. At pH 7, the surface site blockage by adsorbed OM at comparable C loadings was less effective, while less aggregated particles were more prone to dissolution. For OM coprecipitated with Fe, there was no distinct accelerating or inhibiting effect on DFOB-promoted dissolution to be found. Initial Fe dissolution rates at given soil conditions were thus affected by both the type of OM and the sorption procedure. Our results therefore corroborate the importance of considering the heterogeneous composition of soil OM when investigating the mobilization of Fe-organic associations.

Changes in the structure of birnessite during siderophore-promoted dissolution: A time-resolved synchrotron X-ray diffraction study

We used time-resolved synchrotron X-ray diffraction to follow the complete dissolution of synthetic triclinic Na-birnessite as promoted by the trihydroxamate siderophore desferrioxamine B (DFOB). Many microorganisms employ siderophores to increase the availability of Fe, Mn, and other trace metals for metabolic processes. Our primary goal was to quantify the DFOB-assisted dissolution rate by direct, continuous observation of the solid phase. Our kinetic model indicates that the rate of dissolution is dependent on [DFOB] but not pH, and has a reaction order of 0.505 with a rate constant of 0.112wt%birnmin−1. The unit-cell dimensions of birnessite remained virtually constant within error throughout the dissolution process, showing only a 0.3% contraction along the c-axis.Despite the small changes in unit-cell volume, Rietveld analysis revealed that the occupancy of Mn within the octahedral sheets decreased from 100% to ~80%, presumably as the result of complexation of structural Mn3+ with DFOB followed by extraction of Mn3+ from the crystal structure. These observations suggest a critical lacunarity of ~20mol% Mn for triclinic Na-birnessite, below which the structure is destabilized. Moreover, this study reveals that DFOB-promoted dissolution must operate by a different mechanism from that engaged when bacterial membrane fractions directly transfer electrons to birnessite crystals. We propose that crystal structure analysis of minerals undergoing dissimilatory metal reduction can elucidate metabolic pathways employed by microorganisms.

Oxidative mobilization of cerium and uranium and enhanced release of “immobile” high field strength elements from igneous rocks in the presence of the biogenic siderophore desferrioxamine B

Polyvalent trace elements such as the high field strength elements (HFSE) are commonly considered rather immobile during low-temperature water–rock interaction. Hence, they have become diagnostic tools that are widely applied in geochemical studies. We present results of batch leaching experiments focused on the mobilization of certain HFSE (Y, Zr, Hf, Th, U and rare earth elements) from mafic, intermediate and felsic igneous rocks in the presence and absence, respectively, of the siderophore desferrioxamine B (DFOB). Our data show that DFOB strongly enhances the mobility of these trace elements during low-temperature water–rock interaction.The presence of DFOB produces two distinct features in the Rare Earths and Yttrium (REY) patterns of leaching solutions, regardless of the mineralogical and chemical composition or the texture of the rock type studied. Bulk rock-normalized REY patterns of leaching solutions with DFOB show (i) a very distinct positive Ce anomaly and (ii) depletion of La and other light REY relative to the middle REY, with a concave downward pattern between La and Sm. These features are not observed in experiments with hydrochloric acid, acetic acid or deionized water. In DFOB-bearing leaching solutions Ce and U are decoupled from and selectively enriched relative to light REY and Th, respectively, due to oxidation to Ce(IV) and U(VI). Oxidation of Ce3+ and U4+ is promoted by the significantly higher stability of the Ce(IV) and U(VI) DFOB complexes as compared to the Ce(III) and U(IV) DFOB complexes. This is similar to the relationship between the Ce(IV)- and Ce(III)-pentacarbonate complexes that cause positive Ce anomalies in alkaline lakes. However, while formation of Ce(IV) carbonate complexes is confined to alkaline environments, Ce(IV) DFOB complexes may produce positive Ce anomalies even in mildly acidic and near-neutral natural waters. Siderophore-promoted dissolution processes also significantly enhance mobility of other ‘immobile’ HFSE and may not only cause or modify Ce anomalies and Th–U fractionation, but also mobilization of and fractionation between Zr, Hf, Th and redox-insensitive REY during weathering, pedogenesis, diagenesis and incongruent dissolution of particles in seawater and freshwater.Siderophores may significantly affect the use of HFSE as geochemical tools. Concave downward light REY patterns may be used as a biosignature for water–rock interaction in the presence of siderophores. Enhanced and preferential mobilization of U relative to Th in the presence of siderophores may produce Th–U signals comparable to those indicative of weathering under oxidized conditions, which might constrain the use of U concentrations and Th/U ratios as a paleoredox-proxy. The enhanced mobilization of Zr and especially Hf from igneous rocks in the presence of DFOB might have implications for the use of the latter as a tracer for the impact of continental weathering on seawater chemistry. Because siderophore complexes affect the particle-reactivity of Hf and Zr, they may prevent effective removal of terrigenous Hf and Zr during aggregation/coagulation of riverine particles in estuaries. Siderophore-promoted solubilization and stabilization might hence be an additional way to transport continental Hf and Zr to the oceans. Furthermore, siderophore-enhanced mobilization may also have implications for the remediation techniques employed to immobilize HFSE such as U, Th and REY, at nuclear waste and reprocessing sites and at REY ore processing plants, where soils are commonly contaminated with these (sometimes radioactive) heavy metals.

Metal oxyhydroxide dissolution as promoted by structurally diverse siderophores and oxalate

Siderophores, a class of biogenic ligands with high affinities for Fe(III), promote the dissolution of metal ions from sparingly soluble mineral phases. However, most geochemical studies have focused on quantifying the reactivity of DFOB, a model trishydroxamate siderophore. This study utilized three different siderophores, desferrioxamine B, rhizoferrin, and protochelin, with structures that contain the most commonly observed binding moieties of microbial siderophores to examine the siderophore-promoted dissolution rates of FeOOH, CoOOH, and MnOOH in the absence and presence of the ubiquitous low molecular mass organic acid oxalate by utilizing batch dissolution experiments at pH=5–9. Metal-siderophore complex and total dissolved metal concentrations were monitored for durations of one hour to fourteen days, depending on the metal oxyhydroxide identity and solution pH. The results demonstrate that MnOOH and CoOOH generally dissolve more quickly in the presence of siderophores than FeOOH. Whereas FeOOH dissolved exclusively by a ligand-promoted dissolution mechanism, MnOOH and CoOOH dissolved predominantly by a reductive dissolution mechanism under most experimental conditions. For FeOOH, siderophore-promoted dissolution rates trended with the stability constant of the corresponding aqueous Fe(III) complex. In the presence of oxalate, measured siderophore-promoted dissolution rates were found to increase, decrease, or remain unchanged as compared to the observed rates in single-ligand systems, depending on the pH of the system, the siderophore present, and the identity of the metal oxyhydroxide. Increases in observed dissolution rates in the presence of oxalate were generally greater for FeOOH than for MnOOH or CoOOH. These results elucidate potential dissolution mechanisms of both ferric and non-ferric oxyhydroxide minerals by siderophores in the environment, and may provide further insights into the biological strategies of metal acquisition facilitated by coordinated exudation of low molecular weight organic acids and siderophores.

Siderophore-promoted dissolution of smectite by fluorescent Pseudomonas.

Siderophores are organic chelators produced by microorganisms to fulfil their iron requirements. Siderophore-promoted dissolution of iron-bearing minerals has been clearly documented for some siderophores, but few studies have addressed metabolizing siderophore-producing bacteria. We investigated iron acquisition from clays by fluorescent Pseudomonads, bacteria that are ubiquitous in the environment. We focused on the interactions between smectite and Pseudomonas aeruginosa, a bacterium producing two structurally different siderophores: pyoverdine and pyochelin. The presence of smectite in iron-limited growth media promoted planktonic growth of P. aeruginosa and biofilm surrounding the smectite aggregates. Chemical analysis of the culture media indicated increases in the dissolved silicon, iron and aluminium concentrations following smectite supplementation. The use of P. aeruginosa mutants unable to produce either one or both of the two siderophores indicated that pyoverdine, the siderophore with the higher affinity for iron, was involved in iron and aluminium solubilization by the wild-type strain. However, in the absence of pyoverdine, pyochelin was also able to solubilize iron but with a twofold lower efficiency. In conclusion, pyoverdine and pyochelin, two structurally different siderophores, can solubilize structural iron from smectite and thereby make it available for bacterial growth.

Siderophore-promoted dissolution of chromium from hydroxide minerals

Biomolecules have significant impacts on the fate and transport of contaminant metals in soils and natural waters. Siderophores, Fe(iii)-binding agents that are exuded by microbes and plants, may form strong complexes with and promote the dissolution of contaminant metal ions, such as Co(iii), U(iv), or Pu(iv). Although aqueous Cr(iii)-siderophore complexes have been recognized in the laboratory setting for almost 40 years, few studies have explored interactions of siderophores with Cr-bearing minerals or considered their impacts on environmental chemistry. To better understand the possible effects of siderophores on chromium mobility, we conducted a series of dissolution experiments to quantify the dissolution rates of Cr(iii)(OH)3 in the presence of hydroxamate, catecholate, and α-hydroxycarboxylate siderophores over a range of environmentally relevant pH values. At pH = 5, dissolution rates in the presence of siderophores are similar to control experiments, suggesting a predominantly proton-promoted dissolution mechanism. At pH = 8, the sorption of the siderophores desferrioxamine B and rhizoferrin can be modeled by using Langmuir isotherms. The dissolution rates for these siderophores are proportional to the surface concentrations of sorbed siderophore, and extended X-ray absorption fine structure spectra of dissolution products indicates the formation of Cr(iii)HDFOB(+) and Cr(iii)rhizoferrin(3-) complexes, suggesting a ligand-promoted dissolution mechanism at alkaline pH. Because siderophores promote Cr(iii)(OH)3 dissolution at rates similar in magnitude to those of iron hydroxides and the resulting Cr(iii)-siderophore complexes may be persistent in solution, siderophores could potentially contribute to the mobilization of Cr in soils and sediments where it is abundant due to geological or anthropogenic sources.

Siderophore-promoted dissolution of cobalt from hydroxide minerals

Recent research has revealed that siderophores, a class of biogenic ligands with high affinities for Fe(III), can also strongly complex Co(III), an element essential to the normal metabolic function of microbes and animals. This study was conducted to quantify the rates and identify the products and mechanisms of the siderophore-promoted dissolution of Co from synthetic Co-bearing minerals. The dissolution reactions of heterogenite (CoOOH) and four Co-substituted goethites (Co-FeOOH) containing different Co concentrations were investigated in the presence of a trihydroxamate siderophore, desferrioxamine B (DFOB), using batch and flow-through experiments. Results showed that DFOB-promoted dissolution of Co from Co-bearing minerals may occur via pH-dependent ligand-promoted or reductive dissolution mechanisms. For heterogenite, ligand-promoted dissolution was the dominant pathway at neutral to alkaline pH, while production of dissolved Co(II) for pH <6. It was not possible from our data to decouple the separate contributions of homogenous and heterogeneous reduction reactions to the aqueous Co(II) pool. Cobalt substitution in Co-substituted goethite, possibly caused by distortion of goethite structure and increased lattice strain, resulted in enhanced total dissolution rates of both Co and Fe. The DFOB-promoted dissolution rates of Co-bearing minerals, coupled with the high affinity of Co(III) for DFOB, suggest that siderophores may be effective for increasing Co solubility, and thus possibly Co bioavailability. The results also suggest that siderophores may contribute to the mobilization of radioactive 60Co from Co-bearing mineral phases through mineral weathering and dissolution processes.

Desferrioxamine-B adsorption to and iron dissolution from palygorskite and sepiolite

Dissolution weathering of minerals can be greatly affected by the presence of siderophores and their adsorption in soil environments. In this research, adsorption equilibria and kinetics of desferrioxamine-B (DFO-B) siderophore on palygorskite and sepiolite, minerals of arid and semiarid soils, were investigated. Iron (Fe) release pattern in the presence of increasing concentrations of DFO-B was also studied. Palygorskite represented a higher capacity but lower affinity for DFO-B adsorption compared to sepiolite. Retention of DFO-B by the minerals was initially rapid and then slowed down as time progressed. Time-dependent DFO-B adsorption to palygorskite and sepiolite was best described by the pseudo second-order and parabolic diffusion models, respectively. The presence of DFO-B enhanced the amount of Fe released from the clay minerals suggesting that siderophore-promoted dissolution might be one of the weathering mechanisms acting on these fibrous clay minerals. Iron concentrations measured in the equilibrium solutions with palygorskite and sepiolite were in the adequate Fe nutrition range for microorganisms and plant roots in soil environments.

Adsorption of hydroxamate siderophores and EDTA on goethite in the presence of the surfactant sodium dodecyl sulfate.

Siderophore-promoted iron acquisition by microorganisms usually occurs in the presence of other organic molecules, including biosurfactants. We have investigated the influence of the anionic surfactant sodium dodecyl sulfate (SDS) on the adsorption of the siderophores DFOB (cationic) and DFOD (neutral) and the ligand EDTA (anionic) onto goethite (α-FeOOH) at pH 6. We also studied the adsorption of the corresponding 1:1 Fe(III)-ligand complexes, which are products of the dissolution process. Adsorption of the two free siderophores increased in a similar fashion with increasing SDS concentration, despite their difference in molecule charge. In contrast, SDS had little effect on the adsorption of EDTA. Adsorption of the Fe-DFOB and Fe-DFOD complexes also increased with increasing SDS concentrations, while adsorption of Fe-EDTA decreased. Our results suggest that hydrophobic interactions between adsorbed surfactants and siderophores are more important than electrostatic interactions. However, for strongly hydrophilic molecules, such as EDTA and its iron complex, the influence of SDS on their adsorption seems to depend on their tendency to form inner-sphere or outer-sphere surface complexes. Our results demonstrate that surfactants have a strong influence on the adsorption of siderophores to Fe oxides, which has important implications for siderophore-promoted dissolution of iron oxides and biological iron acquisition.

Effects of anionic surfactants on ligand-promoted dissolution of iron and aluminum hydroxides

We investigated the influence of the surfactants sodium dodecyl sulfate (SDS) and rhamnolipid (RhL) on ligand-promoted dissolution of goethite ( α-FeOOH) and boehmite ( γ-AlOOH) at pH 6. The siderophore desferrioxamine B (DFOB), its derivate desferrioxamine D (DFOD), ethylenediaminetetraacetic acid (EDTA), and 8-hydroxyquinoline-5-sulfonic acid (HQS) were used as ligands. The rates of ligand-promoted dissolution of goethite were significantly increased in the presence of low concentrations of anionic surfactants (<80 μM SDS; <6 mg/L RhL). At higher surfactant concentrations, however, the effects of surfactants were negligible. The dissolution rates in the presence of surfactants were not correlated with adsorbed amounts of ligands. Three possible factors contributing to these observations were further investigated and discussed: (i) adsorbed surfactants may influence ligand adsorption by changes in the ligand's surface speciation, (ii) re-adsorption of Fe–DFOB or Fe–DFOD complexes may lead to an underestimation of siderophore-promoted dissolution rates at high surfactant concentrations, and (iii) co-adsorption of protons to goethite with SDS may influence the dissolution rates. However, our results show that none of these three factors can satisfactorily explain the observed effects of anionic surfactants on ligand-promoted dissolution rates of iron and aluminum hydroxides.

Synthetic coprecipitates of exopolysaccharides and ferrihydrite. Part II: Siderophore-promoted dissolution

Ferrihydrite (Fh) coprecipitated with exopolymers of plants and microbes may differ in its geochemical reactivity from its abiotic counterpart. We synthesized Fh in the presence and absence of acid polysaccharides (polygalacturonic acid (PGA), alginate, xanthan) and characterized the physical and structural properties of the precipitates formed [Mikutta C., Mikutta R., Bonneville S., Wagner F., Voegelin A., Christl I. and Kretzschmar R. (2008) Synthetic coprecipitates of exopolysaccharides and ferrihydrite. Part I: Characterization. Geochim. Cosmochim. Acta]. In this paper, we focus on the reactivity of PGA and alginate coprecipitates and pure Fh, and studied their interaction with the microbial siderophore desferrioxamine B (DFOB) in the presence and absence of low molecular weight organic (LMWO) acid anions (malate, citrate). Batch adsorption and dissolution experiments were performed in the dark at pH 7 in 10 mM NaClO 4 background electrolyte. In the dissolution experiments, different modes of ligand addition were applied (single, simultaneous, stepwise). With an estimated Langmuir sorption maximum of 15 mmol/mol Fe, a PGA coprecipitate with 11% C org sorbed about four times as much DFOB as pure Fh, and the amount of DFOB sorbed was ∼4-fold larger than estimated from the sum of DFOB sorption to pure Fh and PGA alone. The apparent initial dissolution rates, R app-initial, and pseudo-first order rate coefficients, k, of the coprecipitates exceeded those of pure Fh by up to two orders of magnitude. Citrate and malate exerted a strong synergistic effect on the DFOB-promoted dissolution of pure Fh, whereas synergistic effects of both anions were absent or negligible for the coprecipitates. R app-initial of the citrate and DFOB-promoted dissolution of PGA coprecipitates increased with increasing molar C/Fe ratio of the coprecipitates, independent of the charge of the LMWO ligand. Our results indicate that polyuronates stabilize Fh particles sterically and /or electrostatically, thus increasing the mineral surface area accessible to LMWO ligands. In contrast, pure Fh was coagulated at pH 7 (pH iep of Fh = 7.1), and hence only a small fraction of the Fh surface underwent dissolution. The increase in ligand-accessible surface area of Fh upon coprecipitation with acid polysaccharides seems to primarily control the kinetics of the ligand-promoted dissolution at neutral pH. In pH environments where the solubility of Fe(III) is very low, dissolution rates of Fe(III) (hydr)oxides in such coprecipitates may therefore exceed those of pure minerals by several orders of magnitude, despite a similar crystallinity of the minerals.

Dissolution of hausmannite (Mn 3O 4) in the presence of the trihydroxamate siderophore desferrioxamine B

That microbial siderophores may be mediators of Mn(III) biogeochemistry is suggested by recent studies showing that these well known Fe(III)-chelating ligands form very stable Mn(III) aqueous complexes. In this study, we examine the influence of desferrioxamine B (DFOB), a trihydroxamate siderophore, on the dissolution of hausmannite, a mixed valence Mn(II, III) oxide found in soils and freshwater sediments. Batch dissolution experiments were conducted both in the absence (pH 4–9) and in the presence of 100 μM DFOB (pH 5–9). In the absence of the ligand, there is a sharp decrease in the extent of proton-promoted dissolution above pH 5 and no appreciable dissolution above pH 8. The resulting aqueous Mn 2+ activities were in good agreement with previous studies, indirectly supporting the accepted two-step mechanism involving the formation of manganite and reprecipitation of hausmannite. Desferrioxamine B enhanced hausmannite dissolution over the entire pH range investigated, both via the formation of a Mn(III) complex and through surface-catalyzed reductive dissolution. Above pH 8, non-reductive ligand-promoted dissolution dominated, whereas below pH 8, dissolution was non-stoichiometric with respect to DFOB. Concurrent proton-promoted, ligand-promoted, reductive, and induced dissolution was observed, with Mn release by either reductive or induced dissolution increasing linearly with decreasing pH. The fast kinetics of the DFOB-promoted dissolution of hausmannite, as compared to iron oxides, suggest that the siderophore-promoted dissolution of Mn(III)-bearing minerals may compete with the siderophore-promoted dissolution of Fe(III)-bearing minerals.

Siderophore-promoted dissolution of synthetic and biogenic layer-type Mn oxides

Siderophores are biogenic chelating agents exuded in terrestrial and marine environments to increase the bioavailablity of ferric iron. Recent work suggests that both solid and aqueous manganese may affect the aqueous speciation of siderophores and thus siderophore-mediated iron transport. Although the interaction of the trihydroxamate siderophore desferrioxamine B (DFOB) with several lower-valence manganese oxides has been studied, the effects of siderophores on Mn(III,IV) oxide dissolution are unknown. To remedy this situation, we measured the dissolution rates of two synthetic layer-type Mn(IV) oxides and a biogenic oxide produced by a model organism, Pseudomonas putida GB-1. For pH 5–7, we find that all minerals studied dissolve by traditional reductive (R1) dissolution, yielding Mn(II); for pH 7–9, dissolution yields Mn(III)–siderophore complexes, either by selective ligand-promoted dissolution of structural Mn(III) or by reduction of >Mn(IV) to >Mn(III) followed by complexation and solubilization of Mn(III) by DFOB. Because reductive dissolution results in siderophore oxidation, manganese oxide dissolution at acidic pH may provide a significant abiotic sink for siderophores in natural waters. At alkaline pH, Mn(III)–siderophore complexes produced may profoundly affect the aqueous speciation of siderophores as well as provide a source of reactive Mn(III) complexes.

The effect of desferrioxamine B on the desorption of U(VI) from Georgia kaolinite KGa-1b and its ligand-promoted dissolution at pH 6 and 25 °C

The pathway of actinides through the soil column hinges on many intricate processes with soil constituents. These processes often involve the bioactivity of the microenvironment conferring the biosphere a crucial role in the natural attenuation of radionuclide contaminants in soils. In order to investigate the bioavailability of uranium, sorption experiments with U(VI) on kaolinite in the presence of an important organic chelator, DFO-B, at pH 6 and 25 °C were performed. Under these conditions uranyl adsorption reached a constant ∼ 70% of which virtually all was subsequently desorbed in the presence of the siderophore. It is reasoned that the almost quantitative desorption is a result of both direct displacement of uranyl surface species by DFO-B adsorption onto the same kaolinite Al edge sites and indirect desorption via thermodynamic disequilibrium between free and surface-complexed U(VI). Estimates suggest that indirect desorption prevails over direct exchange processes in the detachment of uranyl surface complexes. Yet, direct desorption and the concept of ligands competing for the same adsorption sites is corroborated by experiments where DFO-B and oxalate were employed to assess a potential synergistic effect on kaolinite dissolution. However, no such effect was observed. Species calculations as well as experiments indicate that DFO-B was preferentially adsorbed. In separate systems, DFO-B and oxalate each caused a ligand-promoted dissolution of kaolinite. This enhancement of dissolution rates is consistent with a mechanism involving ligand adsorption rather than chemical affinity or aluminum inhibitory effects. Further support for this hypothesis comes from the observation that siderophore-promoted dissolution of kaolinite showed the same relationship with aqueous ligand concentration as does the surface coverage: At low aqueous DFO-B concentrations < 100 μM increases in surface coverage and dissolution rates are more pronounced than at aqueous DFO-B concentrations > 100 μM, where increase in these parameters is only marginal. The results show that DFO-B is a very efficient U-desorbent and affects uranium mobility in clay containing soils. Moreover, the ligand-promoted desorption results principally in a stable neutral aqueous species (UO 2DFOBH) not likely to re-adsorb on soil particles to a great extent. Hence, the siderophore effect on the bioavailability of U(VI) is not exclusively determined by its desorptive strength but also encompasses the aqueous speciation that follows desorption.

Low Concentrations of Surfactants Enhance Siderophore-Promoted Dissolution of Goethite

Surface-active agents (surfactants) are released by many soil bacteria and plant roots and are also important as environmental contaminants. Their presence at interfaces could influence important biogeochemical processes in soils such as ligand-controlled dissolution, an important process in biological iron acquisition. To investigate their potential influence on ligand-controlled dissolution of iron oxides, we studied the dissolution kinetics of goethite (alpha FeOOH) at pH 6 in the presence of the bacterial siderophore desferrioxamine B (DFOB) and the anionic surfactant sodium dodecyl sulfate (SDS). The adsorption isotherm of SDS on goethite showed an increase in the slope at concentrations ranging between 300 and 400 microM SDS in solution. This increase in slope suggested the onset of admicelle formation. Adsorption of DFOB onto goethite increased strongly with increasing concentrations of adsorbed SDS. Small concentrations of SDS (5 microM) resulted in a 3-fold acceleration of DFOB-controlled goethite dissolution in the presence of 80 microM DFOB, compared to the suspensions without SDS. The effects of SDS on the goethite dissolution rates were less pronounced at higher SDS concentrations, and became negligible above 600 microM total SDS. The dissolution rates of goethite were not proportional to the adsorbed DFOB concentrations, as would be expected for ligand-controlled dissolution. We speculate that increasing concentrations of adsorbed SDS result in a change in DFOB surface speciation from inner-sphere to outer-sphere complexes and, consequently, the ligand-controlled dissolution rates are not linearly related to the adsorbed DFOB concentration. Our results provide the first evidence for an important role of biosurfactants in biological iron acquisition involving siderophores.

Etch pit formation on iron silicate surfaces during siderophore-promoted dissolution

Understanding the effects of microbiota on mineral alteration requires the ability to recognize evidence of bacteria-promoted dissolution on mineral surfaces. Although siderophores are known to promote mineral dissolution, their effects on mineral surfaces are not well known. We have utilized atomic force microscopy (AFM), X-ray photoelectron spectroscopy (XPS), and Mirau vertical scanning interferometry (VSI) to investigate surfaces after incubation with the siderophore desferrioxamine-B mesylate (DFAM) and under colonies of bacteria. Iron-silicate glass planchets chemically similar to hornblende were incubated in buffered growth medium with siderophore-producing bacteria ( Bacillus sp.) for 46 days with parallel abiotic experiments conducted with and without 240 μM DFAM, with and without 0.01 g l − 1 of microbially produced extracellular polysaccharides (EPS, alginate or xanthan gum). Some glass planchets were protected by dialysis tubing from direct contact with the EPS. Weekly sampling and analysis of all filtered sample solutions showed negligible Fe and Al release in the control experiments and significant release of Fe and Al in the presence of DFAM, with negligible changes in pH. Concentration of Fe in the filtered solutions after incubation with bacteria was below detection, consistent with uptake of Fe by cells. Release of Fe, Al, and Si in control, xanthan-only, and alginate-only experiments was negligible. Release of these elements was enhanced in all experiments containing DFAM, and greatest in alginate + DFAM experiments. AFM and VSI analyses reveal widespread, small etch pits and greater root mean squared roughness on siderophore-exposed surfaces and fewer, localized, larger etch pits on bacteria-exposed surfaces. This is the first documented case of etch pit development during siderophore-promoted dissolution. Roughness was not affected by the growth medium, alginate, or xanthan gum alone. The roughness trends among samples correlate with trends in Fe depletion documented by XPS. Enhanced dissolution and roughness cannot be attributed to direct contact with EPS because no significant chemical or physical differences were observed between surfaces directly exposed to EPS and those protected by dialysis tubing. Acetate released from the EPS may have enhanced the siderophore-promoted dissolution. Siderophores produced by Bacillus sp. may be responsible for some of the ‘biopits.’ The difference in size and distribution of the biopits may be related to colonization.

Uptake of Trace Metals and Rare Earth Elements from Hornblende by a Soil Bacterium

Analysis of trace elements released from hornblende between pH 6.5 and 7.5 in the presence of Arthrobacter sp. shows that Fe, Ni, V, Mn, and, to a lesser extent, Co are preferentially released into solution relative to bacteria-free experiments. This enhanced release into solution could be due to contributions from the slightly lowered pH, the presence of low molecular weight organic acids (LMWOAs), or the presence of a catecholate siderophore in experiments with bacteria. The best explanation for enhanced metal release is siderophore complexation at the mineral surface followed by release to solution. However,the relative rates of metal release to solution in these experiments do not strictly follow the trend predicted by the relative ordering of metal hydrolysis, which might be predicted for siderophore-promoted dissolution. For some of these metals, release to solution is fast initially in biotic experiments, but concentrations in solution reach a steady state value or decrease with time as the bacteria cell numbers increase exponentially. Lack of enhanced release to solution for some metals and decreases in release rate with time for others may be explained by uptake into bacteria. Many of the metals predicted to strongly complex with siderophore (including Al, Ti, Fe, Cu) are heavily taken up into cellular material. The relative ordering of organic ligand-element complexation may therefore partially explain the relative ordering of uptake of trace metals and rare earth elements into cell material. Fractionation of heavy rare earth elements taken up into cellular material is also very strong, and increases from Ho to Lu. Strong fractionation in uptake of some elements by bacteria may create biological signatures either in the mineral substrate or in any mineral precipitates associated with the cellular material.

Siderophore-promoted dissolution of hematite

Siderophores are highly Fe( III)-specific bidentate ligands excreted by aerobic and facultative anaerobic microorganisms to facilitate Fe uptake in oxic environments. These compounds are thought to influence mineral weathering and the biogeochemical cycling of Fe, but quantitative information concerning this possible influence is nonexistent. Preparative quantities of a soil bacterium siderophore were extracted and purified for use in batch dissolution experiments performed with synthetic hematite particles suspended in 1 mmol dm −3 NaNO 3 at pH 3 under exclusion of light. The initial siderophore concentration used, 0.24 mmol dm −3 was representative of microniche environments. Soluble Fe per unit mass of hematite was linear with time over an observational period between 2 and 24 h, leading to an area-based dissolution rate of 10 −8 mol m −2 h −1 . Comparative dissolution experiments, performed with oxalate and ascorbate ligands at the 2–3 mmol dm −3 initial concentration typical of soil environments (otherwise identical conditions to the siderophore experiments), led to dissolution rates of 5 X 10 −8 mol m −2 h −1 , in agreement with literature values. The comparability of dissolution rates for a soil bacterium siderophore and two terrestrial organic ligands, despite an order-of-magnitude difference in their initial concentrations, suggests that siderophores may indeed figure significantly in Fe(Ill) -mineral weathering reactions under natural conditions.