Sorption of ferric iron from ferrioxamine B to synthetic and biogenic layer type manganese oxides

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Geochimica et Cosmochimica Acta 72 (2008) 3371–3380 www.elsevier.com/locate/gca

Sorption of ferric iron from ferrioxamine B to synthetic and biogenic layer type manganese oxides Owen W. Duckworth a,*, John R. Bargar b, Garrison Sposito c b

a Department of Soil Science, North Carolina State University, Raleigh, NC 27695-7619, USA Stanford Synchrotron Radiation Laboratory, 2575 Sand Hill Road, Building 137, MS 69, Menlo Park, CA 94025, USA c Division of Ecosystem Science, University of California, Berkeley, CA 94720-3114, USA

Received 6 February 2008; accepted in revised form 23 April 2008; available online 6 May 2008

Abstract Siderophores are biogenic chelating agents produced in terrestrial and marine environments that increase the bioavailability of ferric iron. Recent work has suggested that both aqueous and solid-phase Mn(III) may affect siderophore-mediated iron transport, but scant information appears to be available about the potential roles of layer type manganese oxides, which are relatively abundant in soils and the oligotrophic marine water column. To probe the effects of layer type manganese oxides on the stability of aqueous Fe–siderophore complexes, we studied the sorption of ferrioxamine B [Fe(III)HDFOB+, an Fe(III) chelate of the trihydroxamate siderophore desferrioxamine B (DFOB)] to two synthetic birnessites [layer type Mn(III,IV) oxides] and a biogenic birnessite produced by Pseudomonas putida GB-1. We found that all of these predominantly Mn(IV) oxides greatly reduced the aqueous concentration of Fe(III)HDFOB+ at pH 8. Analysis of Fe K-edge EXAFS spectra indicated that a dominant fraction of Fe(III) associated with the Mn(IV) oxides is not complexed by DFOB as in solution, but instead Fe(III) is specifically adsorbed to the mineral structure at multiple sites, thus indicating that the Mn(IV) oxides displaced Fe(III) from the siderophore complex. These results indicate that layer type manganese oxides, including biogenic minerals, may sequester iron from soluble ferric complexes. We conclude that the sorption of iron–siderophore complexes may play a significant role in the bioavailability and biogeochemical cycling of iron in marine and terrestrial environments. Ó 2008 Elsevier Ltd. All rights reserved.

1. INTRODUCTION Manganese oxides are a ubiquitous component of marine and terrestrial environments, occurring as more than thirty different phases (Post, 1999). The biologically mediation oxidation of Mn(II) is an important process that drives the formation of layer type Mn(III,IV) oxides, common components of soils and natural waters (Tebo et al., 2004). The resulting oxides (nominal chemical formula MnO2), typically possess abundant structural defects (Burns, 1976; Villalobos et al., 2006), high surface areas (Villalobos et al., 2003), and low points of zero charge

*

Corresponding author. E-mail address: [email protected] (O.W. Duckworth). 0016-7037/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.gca.2008.04.026

(Murray, 1974). These structural factors result in high sorptive capacities for metals (Jenne, 1968; Murray, 1975; Nelson and Lion, 2003; Hochella et al., 2005; Villalobos et al., 2005; Toner et al., 2006). Because of their abundance in soils (McDaniel and Buol, 1991; McBride, 1994), rivers (Hochella et al., 2005), wetlands (La Force et al., 2002), and the marine water column (Landing and Bruland, 1980; Yeats et al., 1992), layered Mn oxides are an important sorbent of metal ions, including Fe, in the many diverse environments. The aqueous chemistry and sorption of trace metals by mineral surfaces can be greatly altered by the presence of siderophores, biologically produced organic compounds that strongly complex Fe(III) (Winkelmann, 1991; Kraemer, 2004) and other hard metal ions (Hernlem et al., 1996, 1999; Kiss and Farkas, 1998). The most well studied siderophore is desferrioxamine B (DFOB), a trihydroxamate

O.W. Duckworth et al. / Geochimica et Cosmochimica Acta 72 (2008) 3371–3380

siderophore produced by terrestrial (Muller and Raymond, 1984; Winkelmann, 1991) and marine microbes (McCormack et al., 2003; Gledhill et al., 2004). The effect of DFOB on the sorption of contaminant metals to mineral surfaces has been extensively studied (Kraemer et al., 1999; Neubauer et al., 2000, 2002; Yoshida et al., 2004; Hepinstall et al., 2005). Though the dominant effect is inhibition of adsorption, under certain conditions (viz. pH ranges which favor electrostatic attraction of the complex to the mineral surface) DFOB can augment metal sorption (Kraemer et al., 1999; Neubauer et al., 2002; Hepinstall et al., 2005). In principle, a number of different interactions may facilitate the sorption of metal–siderophore complexes: (1) sorption of an intact complex Fe(III)HDFOB+ complex; (2) specific binding of the siderophore to both the metal and the surface (a type B ternary complex); and (3) dissociation of the complex followed by the sorption of the metal, with several possible fates of the siderophore [e.g., mineral dissolution, sorption, or degradation (Duckworth and Sposito, 2005b)]. Despite this interest in DFOB-contaminant complexes, little is known about the interaction of the ferric complex (ferrioxamine B) with surfaces, which may be significant to the biological transport and uptake of iron. Ferrioxamine B has been shown to adsorb to calcium montmorillonite by intercalation of the intact complex (Siebner-Freibach et al., 2004, 2006). However, the effect of reactive oxide surfaces on the siderophore-mediated transport of iron, which may provide surface binding sites that compete for iron and siderophores, has not been considered. To that end, we examine the sorption of ferrioxamine B, here defined as the sum of processes 1–3 described above, to two synthetic layer type Mn oxides (birnessites) and a biogenic layer type oxide produced by the model organism Pseudomonas putida GB-1. 2. METHODS 2.1. Materials The DFOB utilized in this study is the mesylate salt ½ðC25 H46 N5 O8 ½NH3 þ ðCH3 SO3 Þ Þ produced under the trade name DesferalÒ. The sample is a gift from the Salutar Corporation. All solutions were made with deionized water with a resistivity of 18.3 MX-cm. Unless otherwise specified, all other chemicals are A.C.S. reagent grade. 2.2. Manganese oxide synthesis and characterization The production of synthetic d-MnO2 and c-disordered H+-birnessite, as well as the growth, harvesting, and washing of P. putida biogenic oxides, are described in detail elsewhere (Duckworth and Sposito, 2007). Our model biogenic oxides are similar in structure to the layered birnessite dMnO2 (Villalobos et al., 2003), but contain an approximately 4:1 ratio of biomass: manganese oxide by dry weight (Toner, 2004). Oxides were characterized to determine phase and crystallinity before and after adsorption experiments. X-ray diffraction patterns (Electronic Annex Fig. 1) collected with an X’Pert Pro X-ray diffractometer (PANalytical, Almelo,

The Netherlands) equipped with a Cu-Ka X-ray source agreed well with literature diffractograms (Villalobos et al., 2003, 2006). After reaction with Fe(III)HDFOB+, the synthetic Mn oxides yielded similar diffractograms with no traces of crystalline iron (hydro)oxide phases; however, ˚ (Villafter reaction, the basal (001) reflection at 7.5–8.5 A alobos et al., 2003) had grown in intensity, suggesting a possible increase in layer stacking. The diffraction pattern of the biogenic oxides was unchanged before and after reaction and showed no evidence of Fe oxides; however, post-reaction biogenic oxides contained a small amount of rhodochrosite (MnCO3) as detected by XRD. A detailed characterization of the pre-reacted oxides used in this study, including their morphology, surface area, composition, and average Mn oxidation number, is presented elsewhere (Duckworth and Sposito, 2007). 2.3. Adsorption of ferrioxamine b to synthetic and biogenic manganese oxides The adsorption of Fe(III)HDFOB+ to birnessite was measured at pH 8 as a function of [Fe(III)HDFOB+]. To initiate an experiment, 0.04 g of synthetic MnO2 (c-disordered H+-birnessite or d-MnO2) and 20 mL of a solution containing 10 mM HEPES buffer, 0.1 M NaCl, and 50– 1000 lM Fe(III)HDFOB+ were added to a 30 mL amber high-density polyethylene bottle, which was then sonicated for 15 min. The sample was shaken at 200 rpm at 25 °C in water bath for 72 h, with the equilibration time chosen from time-dependent adsorption experiments conducted at pH 7 (Fig. 1). The suspension was then extracted by syringe and filtered through a 0.22 lm polyethersulfone syringe filter (Millipore), with the first 5 mL of filtrate discarded. Drift in pH was <0.7 during the course of all experiments. Each experiment was performed in triplicate, with a control experiment containing identical solutions without MnO2. The filtrate was analyzed spectrophotometrically for Fe(III)HDFOB+ (e310 = 560 ± 20 M1 cm1; e425 = 2600 ± 50 M1 cm1) and Mn(III)HDFOB+ (e310 = 2060 ±

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120 100 80 60 40 20 0

0

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Fig. 1. Time course of the sorption of Fe(III)HDFOB+ to d-MnO2 at pH 7 and 0.1 M NaCl. A small concurrent release Mn is also shown. Conditions: 2 g/L d-MnO2, 200 mM Fe(III)HDFOB+, 0.1 mM NaCl, initial pH 7. Symbols: closed squares, Fe(III)HDFOB+; open squares, FeT; closed triangles, Mn(III)HDFOB+; open triangles, MnT.

Sorption of ferric iron from ferrioxamine B to manganese oxides

20 M1 cm1; e425 = 330 ± 10 M1 cm1) (Duckworth and Sposito, 2005a,b). Total metal concentration was quantified by ICP-OES (Perkin-Elmer Optima 5300 inductively coupled plasma- optical emission spectrophotometer; Wellesley, MA) using emissions lines 257.61, 259.37, and 260.57 for Mn, and 238.2, 239.5, 240.4, 259.8, 259.9, and 260.7 nm for Fe. A scaled-up version of this procedure, containing 20 g L1 of MnO2 with the solid: Fe(III)HDFOB+ ratio preserved, was used to prepare larger volumes of synthetic MnO2 samples for EXAFS analysis. Similar experiments were conducted for biogenic oxides. The washed solids from a 2-L growth reactor (either cells with biogenic oxides or cells grown without manganese) were diluted with 20 mM HEPES buffer and 0.1 M NaCl, set to the desired pH with NaOH, and diluted to 50 mL in a graduated cylinder. For cells grown with manganese, this brought the Mn-oxide loading to 2.1 ± 0.3 g L1, as determined by the digestion of 1 mL suspension in HNO3 and oxalic acid, quantification of total Mn by ICP-OES, and the assumption of the structural formula MnO2. The suspension was shaken vigorously for 1 h, and 10 mL aliquots were pipetted into 30 mL amber high-density polyethylene bottles. Samples were spiked with 0.1–1 mL of a known concentration (photometrically determined) Fe(III)HDFOB+ solution. These bottles were then placed in a 25 °C water bath and shaken at 200 rpm for 72 h. The samples were then transferred to 50 mL polycarbonate centrifuge tubes, and centrifuged at 26,890g RCF for 30 min. The supernatant solution was then drawn off by syringe and filtered through a 0.22 lm polyethersulfone syringe filter (Millipore), with the first 3 mL of filtrate discarded. This solution was then analyzed for Mn(III)HDFOB+ and Fe(III)HDFOB+ by UV–visible spectroscopy, and for total Fe and Mn by ICP-OES. Samples were conducted in duplicate with a solid-free control and a Fe(III)HDFOB+ free analytical blank. 2.4. X-ray spectroscopy of aqueous and sorbed metal– hydroxamate complexes Fe K-edge transmission and fluorescence-yield (FY) spectra of a solution containing Fe(III)HDFOB+ at pH 9 were measured at SSRL Beamline 11–2 at room temperature using a Lytle-type ionization chamber detector; Fe K-edge FY spectra of Fe-doped d-MnO2 and Fe-DFOB sorbed to birnessites were measured at Beamline 11–2 at room temperature with a 30 element Ge detector array using 100 lm of Al to preferentially attenuate Mn K-a emission. Reference transmission spectra of siderite (FeCO3) and 50 mM FeCl3(aq) were collected at SSRL Beamline 2–3 at room temperature. 2.5. Structural modeling of EXAFS spectra of aqueous and sorbed metal–hydroxamate complexes Spectra were background subtracted, splined, and fit in ˚ using the SIXPack R-space over the range R = 1–6 A interface (Webb, 2005), which makes use of the IFEFFIT engine (Newville, 2001). Amplitude and phase functions were derived from fitting spectral data by use of the

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FEFF6l code with single-scattering paths. The amplitude reduction factor S0 2 was fixed at 0.87 for all shells based on spectral fits for the model compounds [FeCO3(s) and 50 mM FeCl3(aq) (not shown)]. The parameter DE0 was floated during optimization, but was linked to a common value for all shells for a given sample. Coordination numbers (N) were fixed for all shells based upon the physical model described below. Interatomic distances (R) were independently optimized for each shell; the Debye–Waller parameters (r2) were floated independently except for Fe– Mn shells, which were linked to a common floated value. Uncertainty in optimized EXAFS parameters is reported as standard deviation. Cerius2 (Accelrys, San Diego, CA) was utilized to create and visualize structural models based on crystallographic parameters for birnessite (Post and Veblen, 1990). Spectra collected for reference compounds and sorption samples were fit to likely structural models. For the ferrioxamine B standard, we employed a three-shell fit (viz. Fe–O, Fe–C/N, and Fe–C backbone, Electronic Annex Fig. 2) based on the known structure of the complex (Edwards and Myneni, 2005). We developed a model for Fe bound to the surface of Mn oxides based on three basic binding sites (Fig. 2) established from studies of Pb and Zn sorption to biogenic Mn oxides (Manceau et al., 2002; Villalobos et al., 2005; Toner et al., 2006; Takahashi et al., 2007): (a) a double edge-sharing (DES) complex (Takahashi et al., 2007); (b) a triple corner-sharing (TCS) complex (Manceau et al., 2002; Villalobos et al., 2005; Toner et al., 2006; Takahashi et al., 2007); and (c) intact Fe(III)HDFOB+ component (e.g., ferrioxamine sorbed to birnessite as type B ternary surface complex, as an outer sphere surface complex, or partitioned into the organic biofilm matrix) (Siebner-Freibach et al., 2006). Substitution of Fe at layer positions (Manceau et al., 1997) was not included in the model because of a ˚ Fe–Mn dislack of evidence for characteristic 2.90 A tances (vide infra). A double-corner-sharing complex bound to edge sites was not considered because of recent work suggesting the prevalence of the DES complex (Takahashi et al., 2007). A three component model containing DES, TCS, and intact ferrioxamine was utilized to fit birnessite samples. To reduce the number of fitted parameters, the R and r2 of the ferrioxamine component were fixed at values determined by the fitting the aqueous Fe(III)HDFOB+, with the corresponding coordination numbers explicitly scaled during fitting from the fitted fraction of Fe contained in DFOB complexes (fDFOB). The sum of the fractions of TCS, DES, and DFOB was set to unity (e.g., fDES + fTCS + fDFOB = 1). In the Fe-doped d-MnO2, fDFOB = 0; in the Fe(III)HDFOB+-reacted synthetic Mn oxides, fDFOB was found to be insignificant (<6%). To improve error estimation, this term was subsequently set to zero for Fe(III)HDFOB+ sorbed to d-MnO2 and c-disordered H+birnessite. Additionally, a sensitivity analysis was conducted; when fTCS or fDFOB were set equal to zero, fits to the Fourier transform visibly worsened, and the reduced v2 and R-factors both increased by 17–56% when compared to the cases where all components were used.

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A

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Triple Corner Sharing (TSC) Complex

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n (mmol kg-1)

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Mn-O NMn-O = 6 R = 2.01 Å Mn-Mn NMn-Mn = 6 R = 3.52-3.62 Å

B

Double Edge Sharing (DES) Complex Mn-O NMn-O = 6 R = 2.01 Å

Mn-Mn NMn-Mn = 2 R = 3.06 Å

Fig. 2. Possible structures of Fe associated with layer type Mn oxides (Villalobos et al., 2005). (A) Sorption of an iron atom above a vacancy defect as TCS complex. (B) Sorption of an iron atom to a particle edge as a DES complex. In all renderings, a single layer of a manganese oxide is shown. Legend: light gray atoms, oxygen; dark gray atoms, manganese; black atom, iron; gray and black circles and represent radii of constant Fe–O and Fe–Mn interatomic distances, respectively. Lines do no necessary pass through all atoms in a shell because some atoms may be on the opposite side of the layer. Oxygen atoms coordinating Fe but not bonded to Mn oxide are omitted for clarity.

3. RESULTS AND DISCUSSION 3.1. Sorption of Fe(III)HDFOB+ to oxides and biogenic oxides Fig. 3 shows isotherms for the adsorption of ferrioxamine B to d-MnO2, c-disordered H+-birnessite, and biogenic oxide + cells. Although Fig. 3 displays [Fe(III)HDFOB+] data, the agreement between measured [FeT] and [Fe(III)HDFOB+] in all cases is within 10%. These differences are within analytical error; however, this discrepancy may lead to larger percentage deviations of sorbed concentrations determined by mass balance. The sorption data for all three solids exhibit L-type sorption behavior. The sorption of both synthetic oxi-

120 100 80 60 40 20 0

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100

200

300 400 500 [Fe(III)HDFOB+] μM

600

700

Fig. 3. Sorption of ferrioxamine B to layer type manganese oxides. Surface excess (mmol kg1) versus aqueous Fe(III)HDFOB+ (lM). Legend: circles, biogenic oxides + cells; triangles, d-MnO2; squares, c-disordered H+-birnessite; diamonds, cells alone, normalized to the hypothetical mass on Mn oxides typically associated with cells in our experiments. Conditions: initial pH 8, 20 mM HEPES buffer, 0.1 M NaCl and 2 g L1 synthetic oxide or 2.1 g L1 biogenic oxide. Drift in pH through the course of the 72 h experiment is less than 0.7 pH units. The agreement between measured [FeT] and [Fe(III)HDFOB+] in all cases is within 10%.

des can be fit to Langmuir isotherms (Sposito, 2008). We find that the maximum surface excess nmax = 90 ± 20 mmol kg1 (0.35 ± 0.08 lmol m2) and 50 ± 10 mmol kg1(0.15 ± 0.03 lmol m2), with Langmuir binding constant K = 0.4 ± 0.2 mM1 and 0.3 ± 0.1 mM1 at I = 0.1 M for d-MnO2 and c-disordered H+-birnessite, respectively. On the basis of an approximate surface site density of 18 sites nm2 for d-MnO2 (Catts and Langmuir, 1986), we estimate that the maximum surface coverage found corresponds to adsorption of ferrioxamine B on approximately 0.5–1% of all surface sites. Adsorption data for the biogenic oxide + cells are fit with a Freundlich isotherm (n [mmol kg1] = [100.6 ± 0.2] [Fe(III)HDFOB+]0.59 ± 0.09), which is commonly used to model sorption to a heterogeneous solid (Stumm and Morgan, 1996). To determine if the biomass (cells and intracellular polysaccharides) associated with the biogenic oxides affects adsorption, control experiments were conducted in which Fe(III)HDFOB+ was sorbed on cells grown in the absence of manganese at total aqueous concentration from 50 to 600 lM. These data, normalized by the hypothetical mass of Mn oxide that would be associated with the cells if they had been grown in presence of manganese, are plotted in Fig. 3. The sorption of Fe(III)HDFOB+ by cells in the absence of biogenic oxides increases linearly with concentration (R2 = 0.99). When compared to the sorption onto biogenic oxides at corresponding pH and concentrations, biomass grown without Mn (and thus without Mn oxides) accounted for 30% of the sorption by the biogenic oxide + cells samples at high loading. The sorption of Fe(III)HDFOB+ complex to the Mn oxide surface of the biogenic oxides is consistent with observations of Templeton et al. (2001) and Toner et al. (2006) who noted that the presence of a biofilm does not block metal sorption to oxide surfaces. Although it is possible P. putida cells take up Fe(III)HDFOB+, the adsorption in the absence of manganese oxides was limited to 15 ± 1% of the total aqueous concentration in all cases.

Sorption of ferric iron from ferrioxamine B to manganese oxides

3.2. Fe K-edge of EXAFS of Fe(III)HDFOB+ and birnessites

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(Fig. 2), containing a shell of six of manganese atoms at ˚ . Both components are found in approxi3.46 ± 0.01 A mately equal abundance in the sample (fDES = 52 ± 9% and fTCS = 48 ± 9%) of the Fe in the sample. In both com˚ do not ponents, oxygen atoms present at R = 3.5–3.6 A contribute significantly to the data, and are thus excluded from the model, as are all other oxygen atoms occurring at distances beyond this oxygen shell. Fig. 4 shows Fe K-edge EXAFS spectra of Fe(III)HDFOB+ sorbed onto manganese oxides (B–D). Qualitatively, the spectra of Fe(III)HDFOB+ sorbed on Mn oxides resemble that of the Fe-doped d-MnO2 standard, with FT ˚ (R + DR). This observation sugpeaks near 2.5 and 3.0 A gests that the dominant form of Fe in the Fe(III)HDFOB+-biogenic oxide samples is either specifically adsorbed to the oxide surfaces or incorporated into the structures. Furthermore, the EXAFS spectra and the Fourier transforms are distinct from those of common iron (hydr)oxide phases (Suzuki et al., 2001; Chatellier et al., 2004; Waychunas et al., 2005) and natural d-MnO2 containing separate Fe-rich domains (Manceau et al., 1992), consistent with the absence of crystalline Fe phases in X-ray diffraction data (Electronic Annex Fig. 1). Additionally, EXAFS spectra differ from those of iron carbonates (Benner et al., 2002) and metals adsorbed to carbonates minerals (Elzinga and Reeder, 2002; Elzinga et al., 2006), suggesting that isomorphic substitution in or sorption to rhodochrosite formed by the reaction of ferrioxamine with biogenic oxide + cells does not significantly affect adsorption. Although it may be initially surprising that Mn oxides competitively remove Fe(III) from the high affinity DFOB complex [log KFe(III)HDFOB+ = 32.02 (Martell et al., 2001)], the observation may be rationalized by noting the high affinity of Mn oxides for both metals (Tebo et al., 2004) and DFOB (Duckworth and Sposito, 2005b, 2007). The thermodynamic drive for the reaction may arise from the concurrent

Fig. 4 shows the Fe K-edge EXAFS spectra of aqueous Fe(III)HDFOB+(A), Fe(III)HDFOB+ sorbed onto manganese oxides (B–E), and Fe-doped d-MnO2 (F). The EXAFS spectra and Fourier transforms of the adsorbed species all are different from the spectrum of Fe(III)HDFOB+, indicating that the local coordination environment of the Fe is significantly altered upon sorption. The aqueous Fe(III)HDFOB+ data can be fit with a three-shell model ˚ , consis(Table 1); a first shell with a R = 2.016 ± 0.006 A tent with expected Fe(III)–O bond distances (Shannon, 1976) with a fixed N = 6 based an octahedral complex; a second shell of three carbon and three nitrogen atoms in ˚ , in the hydroxamate moieties with a R = 2.84 ± 0.01 A good agreement with published values (Edwards and Myneni, 2005). A third shell, representing the diffuse signal of the carbon/nitrogen backbone, occurs at R = 4.41 ± 0.04, slightly longer than reported by Edwards and Myneni (2005). This difference may be because they fit 12–15 carbon atoms, whereas our approach attempts to capture the average position of the entire 25-atom C/N backbone of the molecule. The Fe-doped d-MnO2 spectrum (F) is qualitatively similar to the published K-edge EXAFS spectra of Ga(III) (Pokrovsky et al., 2004), a trivalent metal with a similar ionic radius to Fe(III) that exhibits two-component behavior, sorbed to d-MnO2, and is consequently fit to a two-component adsorption model. For both components, the first shell is composed of oxygen atoms with an average interatomic ˚ ) that is in good agreement distance (R = 1.994 ± 0.008 A with the expected value for Fe(III)–O bonds (Shannon, 1976). The first component is a DES Fe sorbed to a particle edge, which contains a pair of manganese atoms at ˚ . The second component is a TCS site R = 2.99 ± 0.02 A above a defect site created by a manganese vacancy

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Fig. 4. Fe K-edge EXAFS spectra and Fourier transform data of Fe standards and ferrioxamine B reacted with layer type manganese oxides. (A) 50 mM Fe(III)HDFOB+(aq); (B) Fe(III)HDFOB+ reacted with biogenic manganese oxide + cells (sample 1, n = 166 mmol kg1); (C) Fe(III)HDFOB+ reacted with biogenic manganese oxide + cells (sample 2, n = 91 mmol kg1); (D) Fe(III)HDFOB+ reacted with cdisordered H+-birnessite (n = 57 mmol kg1); (E) Fe(III)HDFOB+ reacted with d-MnO2 (n = 66 mmol kg1); and (F) 20% Fe-doped dMnO2. Black lines are experimental data and open circles are fits based on structural modeling.

0.002

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3.42 ± 0.03 0 3.47 ± 0.02 0 3.00 ± 0.01 0.004 ± 0.001 0.21 ± 0.07 6 2.92 ± 0.02 0.004 ± 0.002 0.17 ± 0.06 6 6 6

sorption of both Fe(III) and DFOB, resulting from the dissociation of complex, onto the abundant surface sites of the Mn oxide. Structural fitting of spectra of Fe(III)HDFOB+ sorbed onto the oxides yields additional quantitative insight into the identity and abundance of surface species. In the case of both synthetic oxides, the dominant species (ca. 80%; Ta˚. ble 1) is a DES species with a Fe–Mn shell at R = 2.9–3.0 A A minor component of Fe sorbed as a TCS complex (20%) ˚ . In both is evident with a Fe–Mn shell at R = 3.42–3.47 A cases, these distances are near the expected values for Fe sorbed at the specific surface site (Fig. 2). A carbon/nitrogen ˚ , characteristic of Fe(III)HDFOB+, is shell at R = 2.84 A not required to fit the synthetic oxide sorption spectra; however, from the EXAFS it is not possible to conclusively rule out weak DFOB association with surficially bound Fe(III) (e.g., by one hydroxamate group as a type A ternary surface complex). Because >Mn(III,IV) (where ‘‘>” denotes a surface) sites that serve as potential high affinity sorption sites for DFOB are in large excess to the surface concentration of adsorbed Fe(III), we postulate that a significant fraction of the DFOB is completely dissociated from Fe. For the biogenic oxide + cell samples, an additional (3rd) species was required to accurately model the EXAFS spectra. Intact Fe(III)HDFOB+ complexes are expected to occur in the cell fraction of these samples (cf., Fig. 2), and this species was added as fit a component based on the optimized structural fit of our Fe(III)HDFOB+ standard. The biogenic oxides samples were thus found to contain fDFOB = 29 ± 15% and 28 ± 15%. The presence of this component is evident in the Fourier transforms of the biogenic oxides samples as a general reduction in amplitude for ˚ caused by a decrease in the fraction of R + DR = 2.0–3.2 A Fe associated with the Mn atoms that occur at these distances and by destructive interference between the EXAFS from the Fe(III)HDFOB+ and DES species. The distribution and structure of the remaining sorbed Fe is similar to that observed in the synthetic layered Mn oxides samples, with approximately 84–86% of the free Fe bound as ˚ . Fits sugDES at edges with an Mn–Mn shell at R = 3.02 A gest that remainder may be sorbed as a TCS over vacancy ˚ . This can defect sites with an Mn–Mn shell at R = 3.47 A not be concluded with certainty, however, due to the relatively large uncertainties on fTCS for these samples. 3.3. Kinetic constraints on the sorption mechanism

2.01

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2.01 ± 0.01 1.96 ± 0.01

0.009 ± 0.001 0.79 ± 0.07 2 0.0094 ± 0.0009 0.83 ± 0.06 2

3.46 ± 0.01 0 2.99 ± 0.02 0.008 ± 0.001 0.48 ± 0.09 6 1.994 ± 0.008 0.0088 ± 0.0006 0.52 ± 0.09 2 6

0 2.016 ± 0.006 0.0034 ± 0.0003 0 6

Fe(III)– HDFOB+ Fe-doped dMnO2 d-MnO2 c-dis. H+birnessite Biogenic Mn ox. 1 Biogenic Mn ox. 2 Expected distances

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RMn–C/N r2Mn–C=N NMn–C RMn–C r2Mn–C ˚) ˚ 2) ˚) ˚ 2) (A (A (A (A NMn–C/N Table 1 EXAFS fitting results

r2Mn–O ˚ 2) (A

fDES

NMn–Mn RMn–Mn (DES) (DES) ˚) (A

r2Mn–Mn (DES) ˚ 2) (A

fTCS NMn–O RMn–O ˚) (A Sample

NMn–Mn RMn–Mn (TCS) (TCS) ˚) (A

fDFOB

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In the case of DFOB-promoted dissolution of Fe and Mn oxides, adsorption of DFOB is typically required to promote dissolution in the absence of secondary reactants (Cocozza et al., 2002; Cheah et al., 2003; Duckworth and Sposito, 2005b). The characteristic time for the DFOB-promoted dissolution of MnO2 in batch systems is on the order of minutes (Duckworth and Sposito, 2007), suggesting the sorption of free DFOB is even more rapid. Because the sorption of the Fe(III)HDFOB+ complex requires >48 h to come to an apparent equilibrium (Fig. 1), we infer that a more complex process than simple adsorption of intact ferrioxamine B occurs. To understand the kinetics of this process, analogy can be drawn to two related processes—

Sorption of ferric iron from ferrioxamine B to manganese oxides

the exchange of Fe(III) from aqueous siderophore complexes and the sorption of ethylenediaminetetraacetic acid (EDTA)–metal complexes to mineral surfaces. The exchange of iron from siderophore complexes is typically a slow process. For example, exchange of Fe(III) from Fe(III)HDFOB+ to EDTA is a slow reaction that occurs via a multistep process that is initiated a partial unwinding of the complexes that is mediated by water and protons (Tufano and Raymond, 1981). Another reaction, the exchange between Fe(III)HDFOB+ and the siderophore ferrichrome B, has been estimated to have a half-life of >200 h at circumneutral pH and equimolar ligand concentration (Tufano and Raymond, 1981). In a related study, Parker et al. (2004) studied the exchange of Fe(III)-pyoverdin (PVD), a microbial siderophore produced by P. putida, with Mn(III)–citrate. This process somewhat analogous to the sorption of Fe(III) to surface and the concurrent sorption of the siderophore to the Mn oxide surface. Although determining the kinetics of the process was not their main objective, the authors note considerable exchange of Mn(III) for Fe(III) after 21 h. The slow kinetics of Fe(III)HDFOB+ sorption is consistent with dissociation of the complex in aqueous phase exchange reactions. The interaction of aqueous EDTA complexes with surfaces may also aid in the interpretation of our kinetic data. A wide range of metal–EDTA complexes have been shown to sorb to aluminum (Bowers and Huang, 1986; Girvin et al., 1993) and iron (hydr)oxides (Nowack and Sigg, 1996), as well as to promote their dissolution. In addition, metal complexed by EDTA can be exchanged from the complex, and the resulting free EDTA can promote the dissolution of iron (hydr)oxides (Nowack and Sigg, 1997). For metals with slow ligand exchange rates (Margerum et al., 1978), the displacement of the chelated metal can be the rate-determining step in the adsorption of EDTA and the subsequent dissolution of the oxide (Nowack and Sigg, 1997). The time required for sorption of the DFOB complex to birnessites suggests that sorption is kinetically hindered by the dissociation of the ferrioxamine B complex, consistent with our spectroscopic observations. 3.4. Environmental implications The ability of manganese oxides to remove Fe(III) from a siderophore complex has profound implications for environmental processes in marine and terrestrial environments. Firstly, the occurrence of manganese oxides in soils, sediments, and the oceans suggests that the sorption of complexed iron to oxide surfaces could compete with siderophore-mediated transport and uptake of iron in many diverse environments. In high nutrient low chlorophyll ocean waters, iron is typical considered to be a limiting nutrient (Coale et al., 1996; Behernfeld and Kolber, 1999). The majority of soluble iron in marine waters has been shown to be in organic complexes (Rue and Bruland, 1995, 1997; Powell and Donat, 2001), and there is a growing consensus that siderophores are a major component of the pool of complexing ligands (Hutchins et al., 1999; Witter et al., 2000; Marcrellis et al., 2001; Butler, 2005; Kraemer et al., 2005). In soils, siderophores are abundant (Powell

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et al., 1980; Holmstro¨m et al., 2004) and have been established as critical components of bacterial, fungal, and plant Fe acquisition systems (Romheld and Marschner, 1986; Marschner and Romheld, 1994; Renshaw et al., 2002; Winkelmann, 2002). The potential of Mn oxides to disrupt this process by removal and sorption of Fe from siderophores may be an important as yet unconsidered constraint on siderophore-mediated iron transport and an additional linkage between the biogeochemical cycling of iron and manganese. The interaction of siderophore complexes with Mn oxides may also provide new insights into the significance of microbial manganese oxidation. Bacteria typically oxidize Mn(II) to form layer type oxides that are closely associated with cells and extracellular polysaccharides (Villalobos et al., 2003; Webb et al., 2005). The underlying purposes of biological Mn oxidation are not known (Tebo et al., 2005); storage of manganese to confer radiation resistance (Daly et al., 2004) and to degrade complex organic matter to metabolically available carbon sources (Sunda and Kieber, 1994) have been suggested as non-metabolic evolutionary advantages. However, biogenic manganese oxides may also play a significant role in biological process by concentrating iron near cells, thus storing Fe for later remobilization by processes such as reductive dissolution by simple metabolites (Stone, 1987; Toner and Sposito, 2005) or reusable electron shuttles (Newman and Kolter, 2000). ACKNOWLEDGMENTS We are grateful to Kenneth Raymond for providing our sample of DesferalÒ. Tim Teague graciously assisted in X-ray diffraction measurements. We thank Edward Bellfield, Elena Pelen, Olivia Dong, Joe Rogers, and Andrew Yang for logistical support, and Jasquelin Pen˜a, Brandy Toner, Dorothy Parker, Treavor Kendall, and Sara Holmstro¨m for valuable discussion. This work was funded by the National Science Foundation, Collaborative Research Activities in Environmental Molecular Science (CRAEMS) program (CHE0089208). Support was also provided by the SSRL environmental remediation sciences program. Portions of this research were carried out at the Stanford Synchrotron Radiation Laboratory, a national user facility operated by Stanford University on behalf of the U.S. Department of Energy, Office of Basic Energy Sciences. The SSRL Structural Molecular Biology Program is supported by the Department of Energy, Office of Biological and Environmental Research, and by the National Institutes of Health, National Center for Research Resources, Biomedical Technology Program.

APPENDIX A. SUPPLEMENTARY DATA Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.gca. 2008.04.026. REFERENCES Behernfeld M. J. and Kolber Z. S. (1999) Widespread iron limitation of phytoplankton in the south pacific ocean. Science 283, 840–843. Benner S. G., Hansel C. M., Wielinga B. W., Barber T. M. and Fendorf S. (2002) Reductive dissolution and biomineraization of iron hydroxide under dynamic flow conditions. Environ. Sci. Technol. 36, 1705–1711.

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Bowers A. R. and Huang C. P. (1986) Adsorption characteristics of metal–EDTA complexes onto hydrous oxides. J. Coll. Int. Sci. 110, 575–590. Burns R. G. (1976) Uptake of cobalt into ferromanganese nodules, soils, and synthetic manganese(IV) oxides. Geochim. Cosmochim. Acta 40, 95–102. Butler A. (2005) Marine siderophore and microbial iron mobilization. BioMetals 18, 369–374. Catts J. G. and Langmuir D. (1986) Adsorption of Cu, Pb and Zn by d-MnO2: applicability of the site binding-surface complexation model. Appl. Geochem. 1, 255–264. Chatellier X., West M. M., Rose J., Fortin D., Leppard G. G. and Ferris F. G. (2004) Characterization of iron-oxides formed by oxidation of ferrous ions in the presence of various bacterial species and inorganic ligands. Geomicrobiol. J. 21, 99–112. Cheah S. F., Kraemer S. M., Cervini-Silva J. and Sposito G. (2003) Steady-state dissolution kinetics of goethite in the presence of desferrioxamine B and oxalate ligands: implications for the microbial acquisition of iron. Chem. Geol. 198, 63–75. Coale K. H., Johnson K. S., Fitzwater S. E., Gordon R. M., Tanner S., Chavez F. P., Ferioli L., Sakamoto C., Rogers P., Millero F., Steinberg P., Nightingale P., Cooper D., Cochlan W. P., Landry M. R., Constantinou J., Rollwagen G., Trasvina A. and Kudela R. (1996) A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature 383, 495–501. Cocozza C., Tsao C. C. G., Cheah S. F., Kraemer S. M., Raymond K. N., Miano T. M. and Sposito G. (2002) Temperature dependence of goethite dissolution promoted by trihydroxamate siderophores. Geochim. Cosmochim. Acta 66, 431–438. Daly M. J., Gaidamakova E. K., Matrosova V. Y., Vasilenko A., Zhai M., Venkateswaran A., Hess M., Omelchenko M. V., Kostandarithes H. M., Makarova K. S., Wackett L. P., Fredrickson J. K. and Ghosal D. (2004) Accumulation of Mn(II) in, Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306, 1025–1028. Duckworth O. W. and Sposito G. (2005a) Siderophore–manganese(III) interactions I. Air-oxidation of manganese(II) promoted by desferrioxamine B. Environ. Sci. Technol. 39, 6037– 6044. Duckworth O. W. and Sposito G. (2005b) Siderophore–manganese(III) interactions II. Manganite dissolution promoted by desferrioxamine B. Environ. Sci. Technol. 39, 6045–6051. Duckworth O. W. and Sposito G. (2007) Siderophore-promoted dissolution of synthetic and biogenic layer type Mn oxides. Chem. Geol. 242, 500–511. Edwards D. C. and Myneni S. C. B. (2005) Hard and soft X-ray adsorption spectroscopic investigations of aqueous Fe(III)– hydroxamate siderophore complexes. J. Phys. Chem. A 109, 10249–10256. Elzinga E. J. and Reeder R. J. (2002) X-ray adsorption study of Cu2+ and Zn2+ adsorption complexes at the calcite surface: implications for site-specific metal incorporation preferences during calcite crystal growth. Geochim. Cosmochim. Acta 66, 3943–3954. Elzinga E. J., Rouff A. A. and Reeder R. J. (2006) The long-term fate of Cu2+, Zn2+, and Pb2+ adsorption complexes at the calcite surface: an X-ray absorption spectroscopy study. Geochim. Cosmochim. Acta 70, 2715–2725. Girvin D. C., Gassman P. L. and Bolton H. (1993) Adsorption of aqueous cobalt ethylenediaminetetraacetate by d-Al2O3. Soil Sci. Soc. Am. J. 57, 47–57. Gledhill M., McCormack P., Ussher S., Achterbeg E. P., Mantoura R. F. C. and Worsfold P. J. (2004) Production of siderophore type chelates by mixed bacterioplankton populations in nutrient enriched seawater incubations. Marine Chem. 88, 75–83.

Hepinstall S. E., Turner B. F. and Maurice P. A. (2005) Effects of siderophores on Pb and Cd adsorption to kaolinite. Clays Clay Min. 53, 557–563. Hernlem B. J., Vane L. M. and Sayles G. D. (1996) Stability constants for complexes of the siderophore desferrioxamine B with selected heavy metal cations. Inorg. Chim. Acta 244, 179–184. Hernlem B. J., Vane L. M. and Sayles G. D. (1999) The application of siderophores for metal recovery and waste remediation: examination of correlations for prediction of metal affinities. Water Resour. 33, 951–960. Hochella M. F., Moore J. N., Putnis C. V., Putnis A., Kasama T. and Eberl D. D. (2005) Direct observation of heavy metal– mineral association from the Clark Fork river superfund complex: implications for metal transport and bioavailability. Geochim. Cosmochim. Acta 69, 1651–1663. Holmstro¨m S. J. M., Lundstro¨m U. S., Finlay R. D. and Van Hees P. A. W. (2004) Siderophores in forest soil solution. Biogeochemistry 71, 247–258. Hutchins D. A., Witter A. E., Butler A. and Luther G. W. (1999) Competition among marine phytoplankton for different chelated iron species. Nature 400, 858–861. Jenne E. (1968) Controls on Mn, Fe, Co, Ni, Cu, and Zn concentrations in soils and water: the significant role of hydrous Mn and Fe oxides. In Trace Inorganics in Water (ed. R. Baker). American Chemical Society, Washington, DC. Kiss T. and Farkas E. (1998) Metal-binding ability of desferrioxamine B. J. Inc. Phenom. Molec. Recog. Chem. 32, 385–403. Kraemer S. M. (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat. Sci. 66, 3–18. Kraemer S. M., Butler A., Borer P. and Cervini-Silva J. (2005) Siderophores and the dissolution of iron-bearing minerals in marine systems. In Molecular Geomicrobiology (eds. J. F. Banfield, J. Cervini-Silva and K. H. Nealson). Mineralogical Society of America, Chantilly, VA. Kraemer S. M., Cheah S. F., Zapf R., Xu J., Raymond K. N. and Sposito G. (1999) Effect of hydroxamate siderophores on Fe release and Pb(II) adsorption by goethite. Geochim. Cosmochim. Acta 63, 3003–3008. La Force M., Hansel C. and Fendorf S. (2002) Seasonal transformations of manganese in a palustrine emergent wetland. Soil Sci. Soc. Am. J. 66, 1377–1389. Landing W. M. and Bruland K. W. (1980) Manganese in the North Pacific. Earth Planet. Sci. Lett. 49, 45–56. Manceau A., Drits V. A., Silvester E., Bartoli C. and Lanson B. (1997) Structural mechanism of Co2+ oxidation by the phyllomanganate buserite. Am. Min. 82, 1150–1175. Manceau A., Gorshkov A. I. and Drits V. A. (1992) Structural chemistry of Mn, Fe, Co, and Ni in manganese hydrous oxides 2. Information from EXAFS spectroscopy and electron and Xray diffraction. Am. Min. 77, 1144–1157. Manceau A., Lanson B. and Drits V. A. (2002) Structure of heavy metal sorbed birnessite. Part III. Results from powder and polarized extended X-ray adsorption fine structure spectroscopy. Geochim. Cosmochim. Acta 66, 2639–2663. Marcrellis H. M., Trick C. G., Rue E. L., Smith G. and Bruland K. W. (2001) Collection and detection of natural iron-binding ligands from seawater. Marine Chem. 76, 175–187. Margerum D. W., Cayley G. R., Weatherburn D. C. and Pagenkopf G. K. (1978) Coordination chemistry. In ACS Monograph 174 (ed. A. E. Martell). American Chemical Society, Washington, DC. Marschner H. and Romheld V. (1994) Strategies of plants for acquisition of iron. Plant Soil 165, 261–274. Martell A. E., Smith R. M., Motekaitis R. J. (2001) NIST critically selected stability constants of metal complexes. NIST, Gathersburg.

Sorption of ferric iron from ferrioxamine B to manganese oxides McBride M. B. (1994) Environmental Chemistry of Soils. Oxford University Press, New York. McCormack P., Worsfold P. J. and Gledhill M. (2003) Separation and detection of siderophores produced by marine bacterioplankton using high-performance liquid chromatography with electrospray ionization mass spectrometry. Anal. Chem. 75, 2647–2652. McDaniel P. A. and Buol S. W. (1991) Manganese distributions in acid soils of the North Carolina piedmont. Soil Sci. Soc. Am. J. 55, 152–158. Muller G. and Raymond K. N. (1984) Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J. Bacterol. 160, 304–312. Murray J. W. (1974) The surface chemistry of hydrous manganese dioxide. J. Coll. Int. Sci. 46, 357–371. Murray J. W. (1975) The interaction of metal ions at the manganese dioxide-solution interface. Geochim. Cosmochim. Acta 39, 505–519. Nelson Y. M. and Lion L. W. (2003) Formation of biogenic manganese oxides and their influence on the scavenging of toxic trace metals. In Geochemical and Hydrological Reactivity of Heavy Metals in Soils (eds. H. M. Selim and W. L. Kingerly). CRC Press, Boca Raton, FL. Neubauer U., Furrer G. and Schulin R. (2002) Heavy metal sorption on soil minerals affected by the siderophore desferrioxamine B: the role of Fe(III) (hydr)oxides and dissolved Fe(III). Eur. J. Soil Sci. 53, 45–55. Neubauer U., Nowack B., Furrer G. and Schulin R. (2000) Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environ. Sci. Technol. 34, 2749–2755. Newman D. K. and Kolter R. (2000) A role for excreted quinones in extracellular electron transfer. Nature 405, 94–97. Newville M. (2001) IFEFFIT: interactive XAFS analysis and FEFF fitting. J. Synchrotron Rad. 8, 322–324. Nowack B. and Sigg L. (1996) Adsorption of EDTA and metal– EDTA complexes onto goethite. J. Coll. Int. Sci. 177, 106–121. Nowack B. and Sigg L. (1997) Dissolution of Fe(III)(hydr)oxides by metal–EDTA complexes. Geochim. Cosmochim. Acta 61, 951–963. Parker D. L., Sposito G. and Tebo B. M. (2004) Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium. Geochim. Cosmochim. Acta 68, 4809–4820. Pokrovsky O. S., Pokrovski G. S. and Schott J. (2004) Gallium(III) adsorption on carbonates and oxides: X-ray absorption fine structure spectroscopy study and surface complexation modeling. J. Coll. Int. Sci. 279, 314–325. Post J. E. (1999) Manganese oxide minerals: crystal structures and economic and environmental significance. Proc. Natl. Acad. Sci. USA 96, 3447–3454. Post J. E. and Veblen D. R. (1990) Crystal structure determinations of synthetic sodium, magnesium, and potassium birnessite using TEM and the Rietveld method. Am. Min. 75, 477–489. Powell P. E., Cline G. R., Reid C. P. P. and Szaniszlo P. J. (1980) Occurrence of hydroxamate siderophore iron chelators in soils. Nature 287, 833–834. Powell R. T. and Donat J. R. (2001) Organic complexation and speciation of iron in the South and Equatorial Atlantic. DeepSea Res. (II Top. Stud. Oceanogr.) 48, 2877–2893. Renshaw J. C., Robson G. D., Trinci A. P. J., Wiebe M. G., Livens F. R., Collison D. and Taylor R. J. (2002) Fungal siderophores: structures, functions, and applications. Mycol. Res. 106, 1123– 1142. Romheld V. and Marschner H. (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80, 175–180.

3379

Rue E. L. and Bruland K. W. (1995) Complexation of iron(III) by natural organic-ligands in the central North Pacific as determined by a new competitive ligand equilibration adsorptive cathodic stripping voltammetric method. Marine Chem. 50, 117–138. Rue E. L. and Bruland K. W. (1997) The role of organic complexation on ambient iron chemistry in the equatorial Pacific Ocean and the response of a mesoscale iron addition experiment. Limnol. Oceanogr. 42, 901–910. Shannon R. (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Cryst. A32, 751–767. Siebner-Freibach H., Hadar Y. and Chen Y. (2004) Interaction of iron chelating agents with clay minerals. Soil Sci. Soc. Am. J. 68, 470–480. Siebner-Freibach H., Hadar Y., Yariv S., Lapides I. and Chen Y. (2006) Thermospectroscopic study of the adsorption mechanism of the hydroxamic siderophore ferrioxamine B by calcium montmorillonite. J. Agric. Food Chem. 54, 1399–1408. Sposito G. (2008) The Chemistry of Soils. Oxford University Press, New York. Stone A. T. (1987) Microbial metabolites and the reductive dissolution of manganese oxides: oxalate and pyruvate. Geochim. Cosmochim. Acta 51, 919–925. Stumm W. and Morgan J. J. (1996) Aquatic Chemistry. Wiley, New York. Sunda W. G. and Kieber D. J. (1994) Oxidation of humic substances by manganese oxides yields low-molecular weight organic substrates. Nature 367, 62–64. Suzuki S., Suzuki T., Kimura M., Takagi Y., Shinoda K., Tohji K. and Waseda Y. (2001) EXAFS characterization of ferric oxyhydroxides. Appl. Surf. Sci. 169, 109–112. Takahashi Y., Manceau A., Geoffroy N., Marcus M. A. and Usui A. (2007) Chemical and structural control of the partitioning of Co, Ce, and Pb in marine ferromagnesian nodules. Geochim. Cosmochim. Acta 71, 984–1008. Tebo B. M., Bargar J. R., Clement B. G., Dick G. J., Murray K. J., Parker D. L., Verity R. and Webb S. M. (2004) Biogenic manganese oxides: properties and mechanisms of formation. Ann. Rev. Earth Planet. Sci. 32, 287–328. Tebo B. M., Johnson H. A., McCarthy J. K. and Templeton A. S. (2005) Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 13, 421–428. Templeton A. S., Trainor T. P., Traina S. J., Spormann A. M. and Brown G. E. (2001) Pb(II) distributions at biofilm– metal oxide interfaces. Proc. Natl. Acad. Sci. USA 98, 11897–11902. Toner B. (2004) The environmental geochemistry of a biogenic manganese oxides. Ph.D., University of California. Toner B., Manceau A., Webb S. M. and Sposito G. (2006) Zinc sorption to biogenic hexagonal-birnessite particles within a hydrated bacterial biofilm. Geochim. Cosmochim. Acta 70, 27– 43. Toner B. and Sposito G. (2005) Reductive dissolution of biogenic manganese oxides in the presence of a hydrated biofilm. Geomicrobiol. J. 22, 171–180. Tufano T. P. and Raymond K. N. (1981) Coordination chemistry of microbial iron transport compounds 21. Kinetics and mechanism of iron exchange in hydroxamate siderophore complexes. J. Am. Chem. Soc. 103, 6617–6624. Villalobos M., Bargar J. R. and Sposito G. (2005) Mechanisms of Pb(II) sorption on a biogenic manganese oxide. Environ. Sci. Technol. 39, 569–576. Villalobos M., Lanson B., Manceau A., Toner B. and Sposito G. (2006) Structural model for the biogenic Mn oxide produced by Pseudomonas putida. Am. Min. 91, 489–502.

3380

O.W. Duckworth et al. / Geochimica et Cosmochimica Acta 72 (2008) 3371–3380

Villalobos M., Toner B., Bargar J. R. and Sposito G. (2003) Characterization of the manganese oxide produced by Pseudomonas putida strain MnB1. Geochim. Cosmochim. Acta 67, 2649–2662. Waychunas G. A., Kim C. S. and Banfield J. F. (2005) Nanoparticulate iron oxide minerals in soils and sediments: unique properties and contaminant scavenging mechanisms. J. Nanopart. Res. 7, 409–433. Webb S. M. (2005) SIXPACK: a graphical user interface for XAS analysis using IFEFFIT. Phys. Scr., 1011–1014. Webb S. M., Tebo B. M. and Bargar J. R. (2005) Structural characterization of biogenic Mn oxides produced in seawater by the marine bacillus sp. strain SG-1. Am. Min. 90, 1342–1357. Winkelmann G. (1991) Specificity of iron transport in bacteria and fungi. In CRC Handbook of Microbial Chelates (ed. G. Winkelmann). CRC Press, Boca Raton.

Winkelmann G. (2002) Microbial siderophore-mediated transport. Biochem. Soc. Trans., 691–696. Witter A. E., Hutchins D. A., Butler A. and Luther G. W. (2000) Determination of conditional stability constants and kinetic constants for strong model Fe-binding ligands in seawater. Marine Chem. 69, 1–17. Yeats P. A., Dalzeil J. A. and Moran S. B. (1992) A comparison of dissolved and particulate Mn and Al distributions in the Western North Atlantic. Oceanol. Acta 15, 609–619. Yoshida T., Ozaki T., Ohnuki T. and Francis A. J. (2004) Adsorption of rare earth elements by c-Al2O3 and Pseudomonas fluorescenscells in the presence of desferrioxamine B: implication of siderophores for the Ce anomaly. Chem. Geol. 212, 239– 246. Associate editor: Stephan M. Kraemer