Systematic investigations on iron cycling in phosphorus/siderophore systems: Synergism or antagonism?

Highlights

• Ferrihydrite dissolution is affected by the presence of siderophores and phosphorus.

• Orthophosphate iron and myo-inositol hexaphosphate iron precipitate at distinct pH.

• The antagonism between P compounds and siderophores largely limits iron release.

Abstract

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 siderophores and phosphorus (P) coexist received little attentions. Current study systematically investigated ferrihydrite 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) potential analysis, sequential extraction analysis (SEDEX), field emission scanning electron microscopy (FESEM), high-resolution transmission electron microscopy (HRTEM), X-ray diffraction (XRD), X-ray photoelectron spectroscopy (XPS), micro Raman spectroscopy and attenuated total reflectance-Fourier transform infrared spectroscopy (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.

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). Siderphores form the most thermodynamically stable complexes because of the high affinity to develop 1:1 hexadentate complexes to Fe(III) (stability 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 conjunction with other organic exudates that coexisted in close associations, 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 electrical field induced by phosphorus binding could attract positively charged siderophore molecules. Elevated surface negative charge density 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 unknown. 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 siderophores. We used the following approaches: 1) we used a fungal siderophore 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 systematically 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.