siderophore systems: Synergism or antagonism?

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Systematic investigations on iron cycling in phosphorus/siderophore systems: Synergism or antagonism? Wenshuai Li *, Xiao-Ming Liu ** Department of Geological Sciences, University of North Carolina-Chapel Hill, NC, USA

A R T I C L E I N F O

A B S T R A C T

Editorial handling by Prof. M. Kersten

Synergisms between microbial exudates on Fe (hydr)oxide dissolution as an effective Fe acquisition pathway have been recently addressed and vigorously debated. However, Fe liberation mechanisms and where side­ rophores and phosphorus (P) coexist received little attentions. Current study systematically investigated ferri­ hydrite dissolution in the presence of desferrioxamine B (DFOB) (a kind of fungally-derived siderophores) and inorganic/organic phosphorus (orthophosphate, Pi; myo-inositol hexaphosphate, IHP), as a function of solute pH, reaction time and reagent content. Reacted solids were characterized by N2-BET adsorption, zeta (ζ) po­ tential analysis, sequential extraction analysis (SEDEX), field emission scanning electron microscopy (FESEM), high-resolution transmission electron microscopy (HRTEM), X-ray diffraction (XRD), X-ray photoelectron spec­ troscopy (XPS), micro Raman spectroscopy and attenuated total reflectance-Fourier transform infrared spec­ troscopy (ATR-FTIR). Our results indicate that upon reaction with P-only or (DFOB + P) systems, interfacial complexation partially switched from monolayer bidentate-binuclear surface complexes to ternary complexes, or laterally transformed into amorphous Fe–P precipitates. The Fe-Pi complex precipitated more readily under acidic conditions, and Fe-IHP complex preferentially nucleated in neutral-alkaline environments. Phosphorus slightly promoted Fe release from minerals and fixation to the leached layer or interfacial liquid zone initially, but subsequently prevented further attacks from protons and DFOB. The co-effects of P and DFOB likely correspond to two successive scenarios: 1) DFOB is preferentially attracted toward ferrihydrite surfaces by negative electrical fields induced by adsorbed phosphorus and can act synergistically with labile P–Fe complexes, resulting in intensive temporal dissolution of Fh; 2) subsequent Fe shuttling to DFOB can be prohibited by stabilized, passive P/Fe–P layers. Our results emphasize the antagonism between P compounds and siderophores (i.e., DFOB here) on ferrihydrite dissolution to improve understanding of the biologically-mediated Fe cycling in natural systems.

Keywords: Ferrihydrite Phosphorus Siderophores Synergism Antagonism Ecology

1. Introduction In natural systems, iron (Fe) is an essential nutrient to organisms (Hersman et al., 2000). Despite of their high abundances in Earth’s crust, soils, sediments, and aquatic systems (Colombo et al., 2014), Fe (hydr) oxides are relatively insoluble (Sullivan et al., 1988) and bioavailable Fe pools derived from Fe (hydr)oxides are commonly far below the needs of plants, fungi, and microorganisms (e.g., Kraemer, 2004; Dehner et al., 2010), resulting in ecological Fe deficiency. In the context of natural Fe acquisition pathway, biogeochemical weathering has been defined as the dissolution of rocks and minerals by physicochemical processes of

microorganisms, plants and deuterogenic biogenic ligands (Shi et al., 2011). Widespread siderophores, as pervasive biogenic chelating agents, are the fundamental biogeochemical weathering strategy developed by the (micro)-biological communities in order to overcome the low abundance of bioavailable Fe in local environments (soils and waters) (Duckworth et al., 2009; Hibbing et al., 2010; Kim et al., 2010). Side­ rphores form the most thermodynamically stable complexes because of the high affinity to develop 1:1 hexadentate complexes to Fe(III) (sta­ bility constants of 1030-1050 (Ahmad and Maathuis, 2014) by hard Lewis base hydroxamate functional groups (Schenkeveld et al., 2016). Recent research have advocated that siderophores usually work in

Abbreviation: Fh, Ferrihydrite; Pi, Orthophosphate; IHP, Myo-inositol hexaphosphate; DFOB, Desferrioxamine B. * Corresponding author. ** Corresponding author. E-mail addresses: [email protected] (W. Li), [email protected] (X.-M. Liu). https://doi.org/10.1016/j.apgeochem.2020.104796 Received 29 December 2019; Received in revised form 16 September 2020; Accepted 23 October 2020 Available online 4 November 2020 0883-2927/© 2020 Elsevier Ltd. All rights reserved.

Please cite this article as: Wenshuai Li, Xiao-Ming Liu, Applied Geochemistry, https://doi.org/10.1016/j.apgeochem.2020.104796

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conjunction with other organic exudates that coexisted in close associ­ ations, and potentially act synergistically in biogeochemical weathering systems (Cordero et al., 2012). Enhancement of synergism on Fe (hydr) oxides dissolution between two distinct organic ligands have been addressed by previous studies (e.g., Stewart et al., 2013; 2016; Wang et al., 2015). There are two prevailing mechanisms responsible for the synergistic effects: 1) Cyclic Fe detachment and Fe(III) shuttling (Akafia et al., 2014; Ito et al., 2011; Wang et al., 2015); 2) Cyclic Fe(III)→Fe(II) detachment, re-oxidation and Fe(III) shuttling (Stewart et al., 2013, 2016; Schenkeveld et al., 2016). Although the effects of fluvic acids and the low-molecule-weight acids such as oxalate and citrate on siderophores-mediated Fe mineral dissolution have been examined (Saad et al., 2017), the role of some bio-essential substances (e.g., phosphorus, sulphur) remained unknown, regardless of their ubiquity on Earth’ surfaces. Soil Fe (hydr)oxides are the major phosphorus (P) adsorbents, particularly in sandy soils, due to a high affinity of P to the active surface of Fe (hydr)oxides (e.g., Borggaard et al., 1990; Kim et al., 2011). The interaction between the P species and Fe (hydr)oxide surface typically results in interfacial complexation (monodentate to bidentate forms), precipitation, and dissolution, which are significant environmental physicochemical processes affecting the eco-environment (Ruttenberg and Sulak, 2011; Li et al., 2013; Feng et al., 2016). Due to its higher surface site density, reactivity and surface/bulk ratio (Hiemstra, 2013), poorly-ordered ferrihydrite (Fh) is often considered as the main source of bioavailable Fe (Kuhn et al., 2014), and the ultimate sink of P in subsurface environments (Khare et al., 2007; Michel et al., 2007). Phosphorus forms a passive interfacial layer that commonly stabilizes Fh (L. Wang et al., 2017a), decreasing Fe bioavailability and limits Fe bio-cycling (Fonseca et al., 2011). Besides, the mineral negative elec­ trical field induced by phosphorus binding could attract positively charged siderophore molecules. Elevated surface negative charge den­ sity increases the electrostatic repulsive pressure between adjacent particles in aggregates, likely providing a basis for Fh dissolution. Interestingly, the possible reductive dissolution induced by redox-active ligands (e.g., hydroxamate groups of siderophores; Akafia et al., 2014) is not shielded by surface P complexes (Latta et al., 2012; Luo et al., 2017). Moreover, siderophores behave as other organic acids that can affect the manner in which P was complexed, i.e., breaking passive P-hosting layers, inducing dissolution (Johnson and Loeppert, 2006). The following hypotheses has been addressed: coupling mechanisms may be analogous to reported synergisms, but the comprehensive effect of siderophores and phosphorus on Fh dissolution should be much complicated. While the syngistisms of siderophores and a wide variety of natural organic acids (e.g., oxalic, citric, fulvic, and humic acids) have been extensively investigated (e.g., Stewart et al., 2013; 2016; Wang et al., 2015), its possible connection with P towards Fh dissolution is still un­ known. Hence, the objectives of this study are to determine the reaction kinetics and mechanisms of P and siderophores on Fh dissolution and differentiate from typical syngistisms between organic acids and side­ rophores. We used the following approaches: 1) we used a fungal side­ rophore desferrioxamine B (DFOB) to represent a common class of siderophores; 2) both inorganic P (Pi, the most common inorganic phosphate) and organic P (IHP, the most abundant organic phosphate in soils; Turner et al., 2002) were studied; 3) we studied the process, mechanism and kinetics of Fh dissolution in the water (P/DFOB-­ free)/single (DFOB/P-only)/binary (P + DFOB) systems; 4) we system­ atically investigated the P binding patterns on Fh surfaces in the single and binary systems via microscopic techniques (FESEM and HRTEM), and spectroscopy techniques (i.e., XRD, ATR-FTIR, μ-Raman); 5) we investigated Fh dissolution as the function of pH, addition sequence, initial P/DFOB concentrations, and experimental duration. Our results provide critical insights in Fe cycling in P-enriched settings during biogeochemical weathering.

2. Materials and experimental setup 2.1. Reagents All chemicals used in this study are reagent-grade or better. Deion­ ized water (18.2 MΩ) was used throughout the experiments and ac­ quired with a Milli-Q element system (Direct-Q® 3UV). Iron (III) chloride hexahydrate salt (purity >99%) was purchased from ACROS ORGANICS™. Sodium phosphate dibasic anhydrous (purity >99.9%) was obtained from Fisher Scientific™. Dipotassium myo-inositol hex­ aphosphate (K2H16(CPO4)6, IHP, purity >95%) and desferrioxamine B mesylate salt (C25H48N6O8⋅CH4O3S, DFOB, purity >92.5%) were from Sigma-Aldrich™. Given the concern of possible hydrolysis of these compounds in solutions, all chemicals were kept in powder forms until experiments were performed. 2.2. Material synthesis The synthesis method of Fh was modified from Dublet et al. (2017). Two-line ferrihydrite (Fh) was prepared by titrating a solution of 0.01 M FeCl3 solution to a pH = 7 ± 0.2 with 1 or 0.1 M NaOH. This was completed within 10 min to avoid akaganeite precipitation (Hansel et al., 2004). After 12 h of equilibration, the Fh suspension was centri­ fuged, filtered, and rinsed with Milli-Q water to remove residual salts. The precipitate was then dried in room temperature and stored at 4 ◦ C for future uses. Because the formulas of Fh, Fe-IHP, and Fe-Pi have not been well explored and vary from one study to another (e.g., Michel et al., 2007), Fh or Fe concentration units (mg⋅L− 1 of Fh or ug⋅L− 1 of Fe) were applied alternatively depending on the literature cited in the following discussion. Brunauer-Emmett-Teller (BET) analysis was performed using a Micromeritics Tristar II 3020 surface area/porosity analyzer (Fig. S1). The calculated BET-N2 surface area of Fh was 205.78 m2/g, consistent with previous reports (e.g., Gustafsson, 2003; Larsen and Postma, 2001). Fe orthophosphate (Fe-Pi) and Fe myo-inositol hexaphosphate (Fe-IHP), severed as references, were synthesized by neutralizing a mixed solution of 0.01 M FeCl3 and 0.01 M P (1:1v/v) to a pH~7 with 0.1 M NaOH. The rest procedures are the same as Fh synthesis step. The precipitates were air-dried at room temperature and stored at 4 ◦ C. 2.3. Batch dissolution experiments We investigated the cooperative effects of DFOB and phosphorus on Fe(III) release using water (P/DFOB-free, A), single (P/DFOB-only, B) and binary (P + DFOB, C) systems at pH of 4–8 considering pH ranges of soils (unlimited soil~4.5; limed soil 6–8; Walter et al., 2017). Experi­ mental settings and procedures are shown in Fig. S2, and Table 1. We performed 30 synchronous experiments (i.e., P and DFOB reagents were added concurrently). The addition sequence of alginate and DFOB has been reported to affect the dissolution if Fe oxides (Wolff-Boenisch and Traina, 2007). To evaluate the contributions of the addition sequence to the overall effect, we adopted two control groups (DFOB was added after two-day reactions between Fh and P, marked as//). The settings include: (a) time series from 15 to 3000 min; (b) pH at 4/6/8; (c) P of 0/0.1/1/10 mM; (d) inorganic and organic P species; (e) DFOB of 0/5/20/50 μM; (f) adding P species and DFOB in Fh suspensions synchronously and asyn­ chronously. In the text, we use [Fe], [P], and [DFOB] to represent the concentration of dissolved Fe, phosphorus, and siderphores, respectively. All experiments were performed in the dark using 50 ml centrifuge tubes with 200 mg Fh in 40 ml un-buffered solutions to mimic watermineral interactions in nature. Before the reactions, prepared Fh sus­ pensions were sonicated for 10 min for particle dispersion. The IHP/ DFOB stock solutions were freshly made to preclude possible hydrolysis. The tubes were shielded with aluminum foil to prevent interferential photochemical redox reactions. A pre-set ionic strength (0.01 M) was 2

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were centrifuged at 16,000×g for 15 min. Sample solutions were syringe filtered (0.22 μm) and stored at 4 ◦ C. Drying step is necessary to remove water, which otherwise overwhelms vibration spectroscopic responses of surface hydroxo groups. The solids were rinsed by Milli-Q water, air-dried, ground, and stored at 4 ◦ C. The description of the analytical methods is given in the Supplementary Information.

Table 1 Experiment setup for Fh-P-DFOB interactions. System

pH

P type

[P] (mM)

[DFOB] (μM)

Time (min)

System A1 System B1 System B2 System B3 System C1 System C2 System C3a System C4 System C5 System C6a

4/ 6/8 4/ 6/8 4/ 6/8 4/ 6/8 4/ 6/8 6

/

0

0

/

0

20

15/30/60/120/180/360/ 720/1440/2160/3000

Pi

0

Pi

0.1/1/ 10 0.1/1/ 10 1

Pi

1

5/20/50

6

Pi

1

20

4/ 6/8 6

IHP

1

20

IHP

1

5/20/50

6

IHP

1

2

IHP

3. Results 3.1. Ligand-mediated solid dissolution

0

Aqueous characterization of dissolution is shown in Figs. 1 and 2, and summarized in Table S1. The Fe dissolution process is generally described by an initial, rapid (often assumed instantaneous) reaction followed by slower kinetic reactions. In the control (P/DFOB-free) (Fig. 1a) and the DFOB-only (Fig. 1b) systems, the dissolution approxi­ mates a typical linear regression following zero-order kinetics far from equilibrium (Lasaga, 2014; Murray and Hesterberg, 2006). Dissolved Fe concentrations increase with reaction time for all the experiments. Negligible amounts of aqueous Fe are detected in alkaline conditions (pH = 8), and it is higher with decreasing pH. The dissolution rate (R) and interception (d) increase from 0.03 to 0.69 g L− 1∙min− 1, and from 23 to 192 μg, respectively, when solute pH changes from 8 to 4. Such a feature suggests a dominant role of proton-driven dissolution at low pH. The presence of DFOB can contribute to Fe mobilization due to strong complexation ability. Dissolution rate (R) increases from 0.28 to 0.71 μg∙L− 1∙min− 1, and interception (d) increases from 128 to 234 μg when pH changes from 8 to 4, consistent with varied charging of Fh and DFOB within the pH range (Fig. S3). In the binary (P + DFOB) systems, the Fe release results are not simply the sum of the two independent surface-controlled ligand-driven dissolutions. Nevertheless, the presence of P combined with DFOB, does not follow the typical synergisms enhancing the Fe release as previously reported (Wang et al., 2015). The amounts of Fe release are positively

20

“/” indicates that P compounds were not added in the system. a DFOB was added after a two-day reaction between Fh and P.

provided by NaCl electrolyte solutions to minimize the influence of electrolyte. The reactors were shaken at 150 rpm and kept at a constant temperature (22.5 ± 0.1 ◦ C) in a Thermo Scientific™ TSSWB 15 water bath. The reaction time was set up to be 50 h to prevent the hydrolysis of organic P on Fe hydroxides (Fang et al., 2018). Reaction solutions were maintained at required pH levels (±0.1) by adjusting the amount of diluted HCl and NaOH solutions. The pH buffers were not adopted for all treatments to minimize the possible formation of Fe or P complexes with buffers and/or particle aggregation behavior (Joshi and Gorski, 2016). Aqueous samples were collected at pre-set time intervals. All samples

Fig. 1. Characterizations of Fh dissolution degrees and kinetics in experimental systems. (A) Iron liberation as a function of time in the water (P/DFOB-free, system A) groups; (B) Iron liberation as a function of reaction time in the single (DFOB-only) system B; (C) Iron liberation as a function of reaction time in the binary (DFOB + Pi) system C; (D) Iron liberation as a function of reaction time in the binary (DFOB + IHP) system C. We note that the mark “//” stands for the lateral addition of DFOB after two-day equilibrium between P reagents and Fh. Linear fittings of Fe dissolution at the initial and late stages are provided. Dissolution rate and the interception are provided in Table S1. 3

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Fig. 2. Hydrochemical characterization of dissolved Fe concentration at the end of experiments in the water (P/DFOB-free, system A), single (P/DFOB-only, system B) and binary (P + DFOB, system C) sets at solute pH of 4–8. We note that the mark “//” stands for the lateral addition of DFOB after two-day equilibrium between P and Fh. P reagents are inorganic (Pi) and organic (IHP) phases.

correlated with DFOB concentration and broadly followed a liner cor­ relation with adsorbed DFOB at pH = 6 (Fig. 1c–d). Although the results suggested a possibility of antagonism at the end of reactions, the dissolution feature can be divided into two stages with distinct linear regressions. During stage (0–180 min), the dissolution rate (R) and interception (d) of binary systems are marginally higher than the sum of

each single system, about 2–3 times higher than these of its equivalent single systems. Above results not only support envisioned initial ligand-driven dissolution during P sorption (Ler and Stanforth, 2003), but also verify a synergistic role of DFOB in favor of directional Fe extraction. The interaction then switches to stage ② (180–3000 min) where the dissolution rate becomes lower than DFOB-only systems. Fe Fig. 3. Hydrochemical characterization of the species-distribution of P from sequential extraction in the water (P/DFOB-free, sys­ tem A), single (P/DFOB-only, system B) and binary (P + DFOB, system C) sets at the so­ lute pH of 4–8. We note that the mark “//” stands for the lateral addition of DFOB after two-day equilibrium between phosphors and Fh. P salts are inorganic (Pi) and organic (IHP). The extractions include crystalline, amorphous, surface-bound, exchangeable and water-soluble P (data listed in Table S2).

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liberation is lower than that in DFOB-only systems. Particularly, these dissolution features are independent of ligand addition sequence). However, when DFOB is added after reaction of P with Fh for 50 h, the Fe release rates in the first stage decrease from 3.1 to 1.7 μg∙L− 1∙min− 1 and 1.8 to 1.2 μg∙L− 1∙min− 1 at pH = 6 (DFOB = 20 μM) in IHP and Pi systems, respectively. Adsorbed DFOB decreases from 14.2 to 12.4 μM and 10.6 to 9.7 μM in IHP and Pi systems. Overall, dissolved Fe at the end of experiments decreases in the presence of P ligands, and positively correlated to solute [P] and [DFOB].

ligands and Fh surfaces. Besides water-soluble P (S1), most of the P (S3) is associated with fractions of Fe hydroxide surface-bound phase (innersphere complex) through chemisorption. Only a minor proportion of P (<2%) are bonded as outer-sphere complex (S2) on the surfaces via physisorption. Notably, it was observed that parts of P (<10%) were fixed into Fe–P nucleation (S4 and S5), mostly in amorphous precipitates (S4). Their concentrations are positively correlated with initial P con­ centrations. The increase in adsorbed Pi is associated with the fractions of metastable Fe-Pi (S4 and S5) in a more acidic environment, while IHP shows a reverse trend. The crystallinity of Fe-Pi is higher than that of FeIHP in our experimental conditions. Hence, the complexation mecha­ nisms of Pi and IHP on Fh surfaces should be different.

3.2. Phosphorus distribution and speciation Speciation analysis of P (both Pi and IHP) in single/binary systems is provided in Fig. 3, and Table S2. The amount of total P in the soluble phases varies from 19% to 62%. Both Pi and IHP show the largest adsorption capacity at pH = 4, while IHP has a higher affinity to Fh surface. The dissolved free P (S1) increases with solute pH, likely reflecting a result of the evolution of electrostatic forces between P

3.3. Microscopic characterization FESEM and HRTEM images of solid samples are shown in Fig. 4. It should be noted that the air-drying process of the sample grids probably affects the aggregation behavior of Fh particles, so the SEM and TEM

Fig. 4. Microscopic characterization of reacted Fh in binary systems ([P] = 1 mM; [DFOB] = 20 μM). (A–B) FESEM images with EDS analysis in binary systems (IHP + DFOB) at pH = 4; (C–D) FESEM images with EDS analysis in binary systems (IHP + DFOB) at pH = 8; (E–F) the FESEM images with EDS analysis in binary systems (PI + DFOB) at pH = 4; (G–H) the FESEM images with EDS analysis in binary systems (PI + DFOB) at pH = 8; (I) HRTEM images in binary systems (IHP + DFOB) at pH = 6. The blue arrow points out newly-formed Fe-Pi precipitates; (J) HRTEM images of Fh in binary systems (Pi/DFOB) at pH = 6. The blue arrow points out newly-formed Fe-IHP precipitates. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 5

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images obtained may not represent the actual particle interactions in the aqueous suspension. Inspection of all samples by SEM after the disso­ lution experiments reveals that the Fh formed in micron-sized aggre­ gates, whereas no significant change is observed in the morphology because of their amorphous forms. Compared with initial Fh and Pi/ DFOB systems, the surface of the post-experiment Fh experienced moderate dissolution in binary (IHP/DFOB) systems at pH = 4. Ferri­ hydrite is kept stable at pH = 8 in both IHP and Pi environments. From EDS spectrums, we observe that the amount of IHP adsorption is less affected by pH variations than that of Pi. HRTEM images show larger aggregates of Fh (100–300 nm) that span a range of aggregate shapes, including elongated, angular aggregates of Fh, spherical aggregates of Fh, and poorly defined aggregate shapes. The fine structures are care­ fully examined by HRTEM. Compared with Fh in P/DFO-free systems, newly-formed nanoplates grown from the edge of Fh are discovered in both binary systems with IHP and Pi, which are similar to the Fe-bearing phosphate minerals reported by Pramanik et al. (2015) and Nan et al. (2011). The formation of Fe–P minerals is further examined in the following sections.

(P/DFOB-free) and the DFOB-only systems, these five peaks are not sensitive to the changes of pH. In the P-only and binary systems, the intensity of 217/284/398 cm− 1 peaks decreases with increasing [P] for both IHP and Pi systems. Specifically, the decrease is more prominent in acidic conditions for Pi, but more significant in alkaline conditions for IHP. Similarly, the other two broad peaks at 490/666 cm− 1 diminish continuously in lower pH for Pi whereas they decrease substantially in higher pH for IHP. Above results may suggest that: 1) The interfacial binding of P can profoundly modify the structure signs of Fh along the surface; 2) the formation of Fe-Pi favors acidic environment, but Fe-IHP is likely to precipitate in alkaline environment. Compared with μ-Raman, ATR-FTIR is more sensitive to the bands with greater dipole moment variances (Specht and Frimmel, 2001), especially for functional groups. The stacked ATR-FTIR patterns of the samples and references are shown in Fig. 6 and Fig. S4. In the water (P/DFOB-free) and the DFOB-only systems, the IR spectra do not change obviously as increasing solute pH. We also observe a minor increase in O–H vibration of adsorbed H2O at 3400/1630 cm− 1 and the C–O v3 modes of carbonate at 1475/1366 cm− 1 (Le Peltier et al., 1998), which is potentially associated with acidic sites changes during deprotonation. In the P-only systems, the spectra for Pi/IHP sorption in the range of 750–1200 cm− 1 is consistent with previous studies. Besides adsorbed H2O and carbonate, the peak areas of Fe–O–P moieties (1024/995 cm− 1 for Pi; 1125/1067/1003 cm− 1 for IHP) and Fe–O–H (890/790 cm− 1) show considerable enhancement in intensity with increasing initial P concentration and decreasing pH, revealing more pronounced Fh-P re­ actions (e.g., monolayer bidentate-binuclear complexation) (Luengo et al., 2006; L. Wang et al., 2017a). An in-situ ATR-FTIR study by Lü et al. (2018) suggested the surface p complexes on Fe (hydr)oxides changed from non-protonated bidentate complex to protonated biden­ tate complex with time. No outer-sphere P complexes at 970/1100 cm− 1 (Liu et al., 2018) were observed. Additionally, it is consistent with P sorption onto Fe (hydr)oxides that initial P concentration and pH do not affect the peak position but the peak area. Similar to the referenced

3.4. Spectroscopic characterization: Raman and FTIR Micro-Raman is highly sensitive to the polarizability of molecular vibrations (Gordon, 1965), especially for the lattice structure in the short wavelength range. The stacked μ-Raman patterns of the samples and references are displayed in Fig. 5, and Fig. S4. The region between 100 cm− 1 and 800 cm− 1 is characteristic of the mineral structure (Gordon, 1965). Three sharp peaks at 217/284/398 cm− 1 well corre­ spond to the lattice modes of 2-line Fh (Mazzetti and Thistlethwaite, 2002). By aligning the patterns with the Raman spectra of Fe–P com­ pounds (this study, Zhang and Brow, 2011), the other two broad and weak peaks at 490/666 cm− 1 are more analogous to non-crystalline Fe-Pi/Fe-IHP phases, which cannot be well-resolved for the vibrations from the phosphate groups or iron-oxygen (Yu et al., 2007). In the water

Fig. 5. Micro-Raman characterization of reacted solids in the water (P/DFOB-free, system A), single (P/DFOB-only, system B) and binary (P + DFOB, system C) sets. Variations in solute pH, [P] and [DFOB] are marked in different colors. Apparent increases in the peak intensities of 490 cm− 1 and 665 cm− 1 (in dotted box) likely correspond to the presence of non-crystalline Fe-Pi/Fe-IHP phases. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) 6

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Fig. 6. ATR-FTIR characterization of reacted solids in the water (P/DFOB-free, system A), single (P/DFOB-only, system B) and binary (P + DFOB, system C) sets. Variations in solute pH, [P] and [DFOB] are marked in different colors. Apparent increases in the peak intensities of in the range of 700–1100 cm− 1 (in dotted box) correspond to the presence of Fe-Pi/Fe-IHP phases, potentially associated with oligomerization and polymerization. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

spectra of Fe-Pi/Fe-IHP, the evolution of P–O–Fe of quantitative sorption is associated with the oligomerization and polymerization reactions (Wang et al., 2017b). 3.5. Spectroscopic characterization: XPS The results of regional/survey scans of binding energy (BE) and the surface atomic mass ratios are shown in Figs. S5–S4. The change in the binding energy of P 2p1/2 is displayed in Fig. 7. The high-resolution scans of the Fe 2p XPS yielded four peaks, including two satellites, i. e., Fe 2p1/2 and Fe 2p3/2 (Grosvenor et al., 2004). This multiplet feature was previously described for Fe (hydr)oxides, like hematite, maghemite, ¨kie et al., 2013; Salama et al., 2015). These peaks are and goethite (Ma caused by the electrostatic interaction between photoionized Fe2p corehole and unpaired Fe3d electron, crystal field interaction, and spin-orbit coupling. Since the electronegativity of P (2.19) is higher than that of Fe (1.83), free electrons will transfer from Fe to P once they are covalently bound. The more positive the Fe atom is, the higher its BE will be. As for Fe 2p1/2 and Fe 2p3/2 peaks in the Pi-only systems, the BE values shift positively from 725.1/710.6 eV to 725.6/711.5 eV with decreasing pH, compared with unreacted Fh of 724.3/710.5 eV. As for Fe 2p1/2 and Fe 2p3/2 peaks in the IHP-only systems, the BE values shifted positively from 725.1/711.6 eV to 726.5/713.7 eV with decreasing pH. In the binary systems, the increasing [DFOB] has little impact on BE of Fe 2p with ±0.2 eV shifts for the IHP and Pi systems. No peaks of structural Fe(II) are found in aerobic conditions. The high-resolution P 2p XPS spectrum can be fitted with two peaks, including P 2p1/2 and P 2p3/2, with a peak interval of 0.8 eV. Because of the electron occupation, P can receive the charge from Fe through Fe/P banding, leading to negative shifts of BE values. It is worth mentioning ¨kie et al., 2013). As for P 2p1/2 that only chemisorption P was found (Ma and P 2p3/2 peaks in the Pi-only systems, the BE values decrease from 133.9/133.1 eV to 133.3/132.5 eV from alkaline to acidic

Fig. 7. XPS characterization of reacted Fh in the water (P/DFOB-free, system A), single (P/DFOB-only, system B) and binary (P + DFOB, system C) sets, displaying the bonding energies of (A) Fe 2p1/2 and (B) P 2p1/2. The starting points denote the bonding energies of pristine Fh and P salts. The addition of inorganic (Pi) and organic (IHP) reagents are marked in red and blue, respec­ tively. We note that changes in the bonding energies of Fe 2p1/2 and P 2p1/2 are discernible to P additions (stage I) and pH (stage II), while are insensitive to the addition of siderophores (DFOB) (stage III). (For interpretation of the ref­ erences to color in this figure legend, the reader is referred to the Web version of this article.)

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environments. The variations in the local coordination environment of P could be inferred from the drastic BE reduction at pH = 4 suggests, likely relevant to the precipitation of Fe-Pi (Yin et al., 2010; Yu et al., 2007). In contrast, the BE values in the IHP-only systems display the maximum at 134.0/133.2 eV, and then decrease to 133.7/132.9 eV with increasing pH. The distinct trend for the IHP systems could be explained by two main mechanisms: 1) free P groups of IHP at acidic conditions exhibit high BE values. According to the equilibrium curves (Fig. S7), IHP is mainly in the form of undissociated molecules under acidic conditions (i. e., more P groups protonated and unoccupied at lower Ph); 2) Fe-IHP of low BE values potentially form at neutral-alkaline conditions, which can be proved by Raman patterns in Fig. 6. In the binary systems, the in­ cremental [DFOB] exerts little impacts on BE values of Fe 2p with ≤0.1 eV shifts. DFOB causes negligible destructions to the surface P complexation.

fixation can be weakened at neutral-alkaline environments; 3) DFOB can only slightly destruct the Fh-P network and increase Fh dissolution; 4) Reductive dissolution induced by DFOB is negligible. These series of processes are consistent with the XAS results of Wang et al. (2017b). Because of the synergistic dissolution kinetics in the initial sorption stage, the temporal unstable Fe–P complexes are likely released to the interfacial liquid zone, followed by ligand exchange with DFOB in wa­ ters. Here, we propose an alternative precipitation mechanism to reason the observation: the growth of amorphous Fe–P unites nucleate in so­ lutions, laterally attachment on Fh surface, and aggregation into 3D nuclei. In addition, the concentration of local P plays a vital role in pro­ moting precipitation. The increasing [P] and released [Fe] in interfacial solution from ligand-dissolution decrease the saturation index of the precipitating of Fe–P. Meanwhile, decreases in interfacial Gibbs free energy Gsurf following the incoming of P inhibit Fh dissolution. It de­ velops to 3D Fe–P spontaneously with a small thermodynamic barrier as expected from the Gibbs equation:

4. Discussion 4.1. Phosphorus surface complexation mechanisms

Gsurf = γ + ​ ΓGads

In classical theory, the chemisorption of P is responsible for the changes in the electric field from ligand-exchange with surface aquo and hydroxo groups (Goldberg and Sposito, 1984). Using infrared spectra and density functional theory (DFT) approached, previous studies sug­ gested that different surface complexes of P can coexist, and the speci­ ation is highly depending on [P], pH, the concentration and reactivity of surface sites (Li et al., 2013). Metal (hydr)oxides, commonly in the form of monodentate complexes, are favored with low surface loading of anions and high pH, while the bidentate-binuclear complexes are prevalent with high surface loading and low pH (Del Nero et al., 2010; Elzinga and Sparks, 2007). The spin-echo mapping of 31P NMR further confirms this conclusion for Pi chemisorption onto goethite, akaganeite, and lepidocrocite (Kim et al., 2011). The results from sequential extractions demonstrate minor outersphere P existing in our experiments. Moreover, we only identified chemisorbed P from XPS BE patterns and ζ potential dynamics. Assignment of the bidentate-binuclear complexes are shown in ATRFTIR spectra (Luengo et al., 2006; L. Wang et al., 2017a), following the classical reaction:

where γ is the intrinsic surface Gibbs free energy (J∙m− 2), which is strongly phase-dependent. Γ is the surface loading (mol∙m− 2), and Gads denotes the Gibbs free energy of adsorption (J∙mol− 1) at given condi­ tions. The contribution of Γ and Gads decreased Gsurf. A significant Gsurf decrease in precipitates Fe–P. Such coupled dissolution-precipitation also occurs during inorganic/organic P adsorption onto Al/Ca/Mgoxides (Sø et al., 2011; Yan et al., 2014a). Considering the exception­ ally low surface Gibbs free energy of Fh (Hiemstra, 2013), the above processes should be more intense. Quantitative thermodynamic analyses are limited because the solu­ bility product data of Fe-Pi and Fe-IHP are unavailable in the literature. Fortunately, the formation of two solids can be directly detected by multi-technique analyses in this study. The continuous growth of the FePi network is favored in acidic conditions, illustrated by the increasing ζ potential over time (Yan et al., 2014b). On the contrary, the ζ potential keeps steady through the interaction processes between IHP and Fh at the given conditions. The 2D-FTIR results suggest that Pi adsorption is more sensitive to pH dynamics in comparison to that of IHP. However, with a long sensitivity to symmetric vibrations, the FTIR results do not provide accurate information of Fe–P precipitates. Peak regions of the complexation between P and Fh for both Pi and IHP increase with decreasing pH, only showing higher adsorption capacity of P with pro­ gressive protonation. Interestingly, Our Raman results reveal that Fe-IHP precipitated in lower pH and Fe-IHP preferentially formed in higher pH, consistent with sequential extractions of P species. Besides, the reductions in BE of XPS P 2p for Pi in pH = 4 and IHP in pH = 6/8, respectively, further confirm the above phenomenon. Furthermore, the 2D-Raman results suggest that Fe-IHP precipitation was more sensitive to pH changes in comparison with Fe-Pi phases. Such contractions can be reconciled by two distinct possible formation mechanisms. As for the precipitation of Fe-Pi, the stronger electric field interaction and the higher adsorption capacity of Pi at acidic conditions result in intensive ligand-driven dissolution favoring the formation of surface ternary complexes and crystallizing progressively in supersatu­ ration state (X. Wang et al., 2017b). Generally, the multiple P groups and strong chelating ability of IHP make the interfacial complexation mechanism different from that of Pi. As for the precipitation of Fe-IHP, the increasing pH makes IHP more deprotonated (pK1-6 = 1.84, pK7,8 = 6.3, pK9-12 = 9.7, Fig. S7), favoring the formation of Fe-IHP complexes. BE reduction in XPS P 2p also confirms that more P groups among the six groups occupied with Fe in an IHP molecule at alkaline conditions. Supportively, Wan et al. (2016) reported similar precipitation processes for Ca-IHP phase on calcite. Accordingly, it is reasonable to infer that the formation of Fe-IHP is strongly linked to the coordination saturation of IHP at neutral-alkaline environments. In sum, upon reaction with P, the

(a− 1)−

≡ FeOH+0.5 + RPOa−4 (aq) + H + (aq) ↔ ≡ (FeO)2 RPO4 2 + H2 O(l) (unbalanced)

(3)

(2)

where R denotes the H atom of Pi or the rest moieties of IHP molecules. However, this simplistic binding pathway cannot explain our observa­ tions. Actually, the raise-drop [Fe] evolution patterns marked in the grey regions in Fig. 1 suggest that the sorption of P on Fh involves a series of processes. Observed P-promoted dissolution is mainly attributed to strong interactions between P groups and surface Fe atoms, inducing covalent bond polarization, and thus reducing the activation energy of Fe leaching. The adsorbed P can impart interfacial strain to the crystal lattice by strong complexion with surface Fe. To release this strain, unstable surface is forced to release Fe3+ into the solution. Therefore, the P binding initiates ligand-driven dissolution, followed by re-fixation of liberated Fe from the leached layer on adsorbed P, eventually forming ternary complexes. The complexes may be converted to stepwise 3-D polymerization (Ler and Stanforth, 2003), as described in a terrace-ledge-link (TLK) model (Sizemore and Doherty, 2009). The development of passive layers preventing Fh surface from further reac­ tion has been previously reported in other systems (Harrison et al., 2015; ¨velmann and Putnis, 2016). Ho Our FTIR and Raman results strongly support that P complexation at the surfaces of Fe (hydr)oxide results in the continuous growth of Fe–P networks. The development of Fe-IHP should be less than Fe-Pi ac­ cording to the BE changes in the pH range. Our XPS data reveal: 1) IHP shows stronger complexation ability with surface Fe; 2) The interfacial P 8

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interfacial complexation on Fh switches from monolayer bidentate-binuclear Fe–P complexes to ternary Fe–P–Fe complexes, or amorphous Fe–P precipitates sequentially in environmentally relevant conditions. We note that the Fe-Pi precipitates more readily in acidic conditions, while Fe-IHP nucleates in neutral-alkaline environments.

(Schenkeveld et al., 2016). However, this mechanism is not adequate to explain what we observed in binary systems because of the absence of other metal competitors. Among examined ligand, those organic acids could solubilize Fe in step (2) to the interfacial liquid zone and passed Fe (III) to DFOB subsequently, consistent to greater stability constant (log β > 30, Crumbliss and Harrington, 2009) for the Fe(III)-DFOB complexes. The above processes keep the “Fe acquisition window” far from equi­ librium (Schenkeveld et al., 2014). However, in this study, Fe concentrations almost reach plateaus after 180 min as a result of surface passivation, shortening the timespan of “Fe acquisition window”. Most likely, this transformation is in close rela­ tionship with the nature of the P, possibly originating from the step (3). Based on FTIR results, Fe(III) minerals can be stabilized in solution by coatings of organic or poly-phosphate (P) after stabilization, with minor destructions from DFOB. The nearly constant BE of P 2p in the binary systems with increasing [DFOB] also supports above conclusion. Although surface P networks do not hinder interfacial electron transfer (Latta et al., 2012; Luo et al., 2017), additional reductive dissolution driven by DFOB (Simanova et al., 2010) should be negligible in this

4.2. Synergistic or antagonistic effects? The interaction of P and Fh can be broadly subdivided into three sequential steps: 1) The ligand-driven dissolution and Fe liberation from the leached layer; 2) the formation of kinetically labile surface ternary complexes and Fe re-adsorption at the leached layer; 3) the stabilization of the ternary complex and/or subsequent nucleation (Fig. 8). With the addition of DFOB, the sustainable synergistic dissolution is established in the organic acids/DFOB systems throughout our experiment, and only temporal synergism occurs in the initial stage of interaction and trans­ forms to an antagonistic effect. Similar contrasts on Fe release occur in the DMA (a phytosiderophore for plant Fe acquisition)/ascorbate sys­ tems due to complexation displacement by other outcompeting metals

Fig. 8. Conceptual framework representing the cooperative effects of Pi/IHP and DFOB on Fh dissolution with changing pH. Both Pi and IHP protect Fh from DFOB attacks in acidic-alkaline conditions. The protective passivation mechanisms of Pi would change from surface precipitation to monolayer surface complexation with pH elevation, whereas IHP follows an opposite pathway. 9

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study because neither Fe(II) nor reductive transformation products are detected. Due to the disruption of Fe shuttling, Cyclic synergistic dissolution cannot continue. In fact, only Fe in the outmost shell can be obtained by DFOB after stabilization, which can be recognized in the binary systems of different addition sequence. The passivation barrier can protect Fe in the inner layer from the further attack of DFOB or proton. The rate coefficients for goethite dissolution by ligands are closely correlated with ligand binding strength (Duckworth and Martin, 2001). The IHP interacts with metal oxides strongly (Feng et al., 2016) with intensive ligand-driven Fe liberation in this study. The noncrystalline metal-IHP complexes observed are intermediate and labile, as discussed in previous research (Wan et al., 2016; Wang et al., 2017b). The Raman results suggest the instability of Fe-IHP with changing solute pH. Additionally, the Raman patterns with perturbation of [DFOB], illus­ trate that the IHP passive layer formed is more sensitive to the attacks from surface DFOB. Hence, the dissolution in the initial stage in the IHP/DFOB systems is synergistic, as indicated by the large dissolution rate coefficient R1 (Table S1). We would like to point out that both Pi and IHP passive complexation layers can protect Fh from the attacks of proton and DFOB, regardless of the dynamic nature of the ligand. In the present case, two distinct scenarios occur sequentially upon reaction with P and DFOB: 1) DFOB could be attracted to the mineral surface by the negative electrical field induced by phosphorus, resulting in initial intensive dissolution via synergistic Fe shutting from labile P–Fe phases to DFOB; 2) further Fe mobilization is prohibited because of the highly recalcitrant nature of surface P/Fe–P layers for appreciable times. In summary, we conclude a long-term antagonism between P and DFOB during Fh dissolution.

To explain why there is no obvious synergistic effect between P and DFOB we suggest several possible reasons: 1) Pi and IHP are commonly non-reductive in nature and redox-inactive to environment perturba­ tions (Borch et al., 2007); 2) the polarizing effect of P is not sufficient to continuously release the structural Fe from mineral lattice (Celi et al., 2003); 3) the adsorption of P will block the surface metal sites, and thus shielding them from the attack of protons or siderophores (Rubasing­ hege et al., 2012); 4) P can form stable surface complexes with surface Fe of high affinity to the Fe (hydr)oxides in long-term relationships (Elzinga and Sparks, 2007), tuning the surface properties of Fh to passivate (Biber et al., 1994), and thus reducing the shuttling kinetics; 5) initially rapid phosphate chemisorption, followed by surface coating from the Fe–P 3D blocks (Putnis, 2014), could hinder the approach of siderophores; 6) the interfacial complexation of P and corresponding crystallization of Fe–P phases can barely be inhibited by siderophores. The above processes are not mutually exclusive, which result in the two-stage dissolution be­ haviors. In sum, we observe a temporary synergistic effect and then it transforms into an antagonistic effect. Our results suggest that the concurrent presence of phosphorus and siderophores slows down Fe biogeochemical cycling. Phosphate can be released to the soil as a result of natural processes and/or anthropogenic activities. Thus, phosphate-induced antagonism enhances Fe deficiency, further affecting the ecosystem suitability. 5. Conclusions This paper attempts to advance the understanding of the presence of phosphorus and siderophores on Fe (hydr)oxide dissolution and to determine the effects of pH, initial P concentration, and the addition sequence in the P and/or DFOB systems. We conclude that organisms are able to create chemically distinct microenvironments (synergism and antagonism), filling a significant knowledge gap in the literature. Moreover, we provide new insights into understanding the biogeo­ chemical cycling of Fe. The main conclusions of this study are summa­ rized as follows:

4.3. Comparison with the reported siderophore-mediated synergistic dissolution Organic exudates from different organism (i.e., plants and/or mi­ crobes) coexisting in close association may act synergistically or antagonistically in natural systems (Cordero et al., 2012; W. Li and Liu, 2020). Previous studies have demonstrated the importance of syner­ gisms of microbial exudates on Fe (hydr)oxide dissolution as an effective biological Fe acquisition pathway. There are commonly two potential strategies for different ligands to acquire Fe: The first one is that organic ligands act as a Fe shuttle to break the integrity of mineral lattice and deliver adjacent Fe(III) to siderophores, exerting a cyclic detachment of a labile pool of OM-Fe(III) surface complexes (e.g., Cervini-Silva and Sposito, 2002; Stewart et al., 2013). The second one is that surface Fe(II) is generated by reductant ligands coupled to Fe(III) reductive dissolution (Huang et al., 2017), and those short-lived surface Fe(II) is then re-oxidized back to Fe(III) (Suter et al., 1991; Deng, 1997). Some organic ligands may act as a redox-active electron donor to reduce surface Fe(III) to Fe(II) under photoirradiation, and then siderophores can deliver the photo-induced Fe(II) into the aqueous phase, thus generating dissolution cycles (Saal and Duckworth, 2010; Wang et al., 2015). This mechanism increases the efficiency of Fe shuttling by siderophores, and subse­ quently facilitates reductive dissolution (Wang et al., 2017b). The presence of siderophores could enhance Fh dissolution by lowering the Gibbs free energy for proton-promoted dissolution, as discussed by Cheah et al. (2003) and Kraemer (2004). DFOB has a positive charge at pH < 8.3 because of the protonation of its terminal amine group (Fig. S7, Martell and Smith, 2004). Compared to the P/DFOB-free systems, we only found slight increases in Fh dissolution in the DFOB-alone systems ascribed to the electrostatic repulsion (Fig. S2). Similar to the functions of those organic acids, surface P can induce a negative electrical field, resulting in positively charged siderophore attraction and better particle separation. In addition, the interactions between P and Fe (hydr)oxides contribute to the ligand-dissolution of Fh during the initial step of adsorption; therefore, synergism between P and DFOB cannot be established in the binary systems.

1. The ability of P complexation onto Fh becomes stronger with decreasing pH. Interfacial complexation partially switches from monolayer bidentate-binuclear complexes to ternary complexes through ligand-driven dissolution and subsequent re-absorption of Fe ions at the leached layer. The ternary complexes may act as the initial nuclei and transform to Fe-Pi precipitates at lower pH, while Fe-IHP precipitates at higher pH during coupled dissolutionprecipitation. Both stabilized surface P complexes and Fe–P pre­ cipitates block the surface metal sites, preventing Fh from proton or siderophore attacks. This inhibiting effect is more pronounced for Pi than IHP, while the presence of DFOB barely affects the integrity of the P/Fe–P layer. 2. Upon reaction with P and DFOB, Fh dissolution occurs in two stages: 1) DFOB is initially attracted to the Fh surface by the negative electrical field induced by adsorbed P. The intermediate labile P/ P–Fe phases cause temporal synergistic dissolution with the presence of DFOB; 2) continuous Fe shuttling by DFOB is prohibited by the passive stabilized P/Fe–P layer, resulting in long-term antagonism on Fe dissolution. The overall Fe dissolution in the binary systems is incongruent and antagonistic. Such substantial surface-controlled antagonism significantly limits Fe bioavailability. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Acknowledgment

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The authors thank the anonymous reviewers and the editor for their valuable comments and suggestions to improve the quality of this paper. This research is supported by the Army Research Office under grant W911NF-17-2-0028. We acknowledge the support of ATR-FTIR and Renishaw inVia Raman microscope spectroscopy in the UNC EFRC Instrumentation Facility established by the UNC EFRC: Center for Solar Fuels, an Energy Frontier Research Center funded by the U.S. Depart­ ment of Energy, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC0001011). XPS, FESEM and HRTEM were per­ formed at the Chapel Hill Analytical and Nanofabrication Laboratory, CHANL, a member of the North Carolina Research Triangle Nanotech­ nology Network, RTNN. UNC CHANL is supported by the National Sci­ ence Foundation, Grant ECCS-1542015, as part of the National Nanotechnology Coordinated Infrastructure, NNCI. We thank Allen F. Glazner (UNC) for providing pXRD instrument, Madelyn Percy (UNC) for pXRD assistance, and Jun Hu (Chem. Dept., UNC) for experiment assistance and discussion. We thank Carrie Lynn Donley (CHANL), Catherine Grace Mckenas (CHANL), Amar Shankar Kumbhar (CHANL), Kyle Brennaman (EFRC) and Ludovic Troian-Gautier (EFRC) for analytical assistance. References Ahmad, I., Maathuis, F.J.M., 2014. Cellular and tissue distribution of potassium: physiological relevance, mechanisms and regulation. J. Plant Physiol. 171, 708–714. https://doi.org/10.1016/j.jplph.2013.10.016. Akafia, M.M., Harrington, J.M., Bargar, J.R., Duckworth, O.W., 2014. Metal oxyhydroxide dissolution as promoted by structurally diverse siderophores and oxalate. Geochem. Cosmochim. Acta 141, 258–269. https://doi.org/10.1016/j. gca.2014.06.024. Borch, T., Masue, Y., Kukkadapu, R.K., Fendorf, S., 2007. Phosphate imposed limitations on biological reduction and alteration of ferrihydrite. Environ. Sci. Technol. 41, 166–172. https://doi.org/10.1021/es060695p. Borggaard, O.K., Jdrgensen, S.S., Moberg, J.P., Raben-Lange, B., 1990. Influence of organic matter on phosphate adsorption by aluminium and iron oxides in sandy soils. Sur. J. Soil Sci. 41 (3), 443–449. https://doi.org/10.1111/j.1365-2389.1990. tb00078.x. Celi, L., De Luca, G., Barberis, E., 2003. Effects of interaction of organic and inorganic P with ferrihydrite and kaolinite-iron oxide systems on iron release. Soil Sci. 168, 479–488. https://doi.org/10.1097/00010694-200307000-00003. Cervini-Silva, J., Sposito, G., 2002. Steady-state dissolution kinetics of aluminumgoethite in the presence of desferrioxamine-B and oxalate ligands. Environ. Sci. Technol. 36, 337–342. https://doi.org/10.1021/es010901n. Cheah, S.F., Kraemer, S.M., Cervini-Silva, J., 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. https:// doi.org/10.1016/S0009-2541(02)00421-7. Colombo, C., Palumbo, G., He, J.Z., Pinton, R., Cesco, S., 2014. Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J. Soils Sediments. https://doi.org/10.1007/s11368-013-0814-z. Cordero, O.X., Ventouras, L.A., DeLong, E.F., Polz, M.F., 2012. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc. Natl. Acad. Sci. U.S.A. 109 https://doi.org/10.1073/ pnas.1213344109, 20059–20064. Dehner, C.A., Awaya, J.D., Maurice, P.A., Dubois, J.L., 2010. Roles of siderophores, oxalate, and ascorbate in mobilization of iron from hematite by the aerobic bacterium pseudomonas mendocina. Appl. Environ. Microbiol. 76, 2041–2048. https://doi.org/10.1128/AEM.02349-09. Del Nero, M., Galindo, C., Barillon, R., Halter, E., Mad´ e, B., 2010. Surface reactivity of α-Al2O3 and mechanisms of phosphate sorption: in situ ATR-FTIR spectroscopy and ζ potential studies. J. Colloid Interface Sci. 342, 437–444. https://doi.org/10.1016/j. jcis.2009.10.057. Duckworth, O.W., Bargar, J.R., Sposito, G., 2009. Quantitative structure-activity relationships for aqueous metal#siderophore complexes. Environ. Sci. Technol. 43, 343–349. https://doi.org/10.1021/es802044y. Duckworth, O.W., Martin, S.T., 2001. Surface complexation and dissolution of hematite by C1-C6 dicarboxylic acids at pH = 5.0. Geochem. Cosmochim. Acta 65, 4289–4301. https://doi.org/10.1016/S0016-7037(01)00696-2. Elzinga, E.J., Sparks, D.L., 2007. Phosphate adsorption onto hematite: an in situ ATRFTIR investigation of the effects of pH and loading level on the mode of phosphate surface complexation. J. Colloid Interface Sci. 308, 53–70. https://doi.org/10.1016/ j.jcis.2006.12.061. Fang, Y., Kim, E., Strathmann, T.J., 2018. Mineral- and base-catalyzed hydrolysis of organophosphate flame retardants: potential major fate-controlling sink in soil and aquatic environments. Environ. Sci. Technol. 52, 1997–2006. https://doi.org/ 10.1021/acs.est.7b05911.

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