The influence of native soil organic matter and minerals on ferrous iron oxidation
Introduction
Iron (Fe) plays a major role in the biogeochemical processes of soils and sediments (Weber et al., 2006, Melton et al., 2014). The redox transformation between Fe(II) and Fe(III) is of particular interest in environments that fluctuate between O2-rich (oxic) and O2-deficient (anoxic) conditions. Under anoxic conditions, Fe(III) oxides, hydroxides, and oxyhydroxides (hereafter termed as Fe oxides) may be reduced by dissimilatory Fe-reducing bacteria coupled to organic matter (OM) decomposition (Lovley and Phillips, 1986, Roden and Zachara, 1996, Konhauser et al., 2011) or reduced abiotically via other reduced species, such as sulfide (Yao and Millero, 1996). Oxidation of Fe(II) is catalyzed abiotically by O2 or by reactive N-species, and biotically by Fe(II)-oxidizing microorganism that use either O2, light, or nitrate to oxidize Fe(II) (Melton et al., 2014). Chemical and biological formation, transformation, and dissolution of Fe-bearing minerals occur at the oxic-anoxic interface, directly impacting Fe bioavailability, and influencing carbon dynamics, nutrient availability, contaminant mobility, and microbial metabolism in soils and sediments (Borch et al., 2010, Li et al., 2012, Riedel et al., 2013, Kleber et al., 2015).
Many soils and sediments undergo redox fluctuations due to rainfall, groundwater-table changes, snowmelt, or irrigation (Silver et al., 1999, Cheng et al., 2010, Liptzin et al., 2011, Schädel et al., 2016, O’Connell et al., 2018), where the temporary influx of dissolved O2 promotes biological or chemical oxidation of Fe(II) and contributes to the formation of Fe-oxides of varying sizes, crystallinity, and purity. In natural environments, the structure, solubility, bioavailability, and relative thermodynamic stability of Fe-oxides vary greatly depending on the biogeochemical conditions during their formation (Cornell and Schwertmann, 2003). Iron oxide mineral formation and transformation are relatively well characterized in synthetic systems. For example, Fe(II) oxidation by dissolved O2 or nitrate-dependent Fe-oxidizing bacteria may result in ferrihydrite (Straub et al., 1996, Banfield et al., 2000, Sodano et al., 2017, Van Groeningen et al., 2020), lepidocrocite (Larese-Casanova et al., 2010b, Chen and Thompson, 2018, Van Groeningen et al., 2020), goethite (Larese-Casanova et al., 2010a, Larese-Casanova et al., 2010b, Chen and Thompson, 2018) or even magnetite formation (Chaudhuri et al., 2001). However, this may not represent their behavior in redox-dynamic soils and sediments in which multiple components interact, including OM and a variety of native mineral surfaces.
There have been a number of laboratory-based studies performed to investigate how O2-mediated, abiotic oxidation of Fe(II) is influenced by dissolved organic ligands such as amino acids (Santana-Casiano et al., 2000), citrate and EDTA (Santana-Casiano et al., 2000, Pham and Waite, 2008, Jones et al., 2015), phthalate and salicylate (Santana-Casiano et al., 2004) and Suwannee River fulvic acid (SRFA) (Rose and Waite, 2002, Pham et al., 2004, Jones et al., 2015). It is clear that dissolved organic materials can either accelerate or retard Fe(II) oxidation depending on the relative strength of their Fe(II)- and Fe(III)-ligand complexes. Reduced dissolved organic matter (DOM) can evidently preserve Fe(II) by functioning as a redox buffer in addition to a complexant or ligand (Daugherty et al., 2017). In addition, Fe(II) oxidation in the presence of dissolved SRFA, leads to the adsorption/co-precpitation of OM with the de novo Fe-oxides, which can further alter the dynamics of Fe(II) oxidation (Chen and Thompson, 2018). It is well recognized that mineral surfaces can act as catalysts for Fe(II) oxidation in synthetic systems designed to degrade hazardous chemicals under anoxic conditions (Buerge and Hug, 1999, Charlet et al., 2002, Chun et al., 2006, Peretyazhko et al., 2008, Larese-Casanova et al., 2010a, Larese-Casanova et al., 2012), by decreasing reduction potential (EH) (Silvester et al., 2005, Stewart et al., 2018) and Gibbs free energy of the reaction (Krumina et al., 2017). Iron oxides are particularly effective in catalyzing Fe(II) oxidation (Tamura et al., 1980, Park and Dempsey, 2005, Joneset al., 2014), because many of them are semiconducting minerals that can facilitate electron transfer in the solid or solid surface to remote locations (Yanina and Rosso, 2008). In addition, mineral surfaces also act as templates that serve as a pattern for the concurrent oxidative mineral growth. When aqueous Fe(II) oxidizes in the absence of minerals, it produces an aqueous Fe(III) complex or metastable Fe minerals (e.g., ferrihydrite or lepidocrocite) (Schwertmann et al., 1984, Chen and Thompson, 2018). In contrast, when Fe(II) oxidizes in the presence of synthetic crystalline Fe-oxides, it commonly forms thermodynamically stable Fe minerals (e.g., goethite or hematite) via epitaxial growth (Chun et al., 2006, Larese-Casanova et al., 2012, Joneset al., 2014, Chen and Thompson, 2018). However, Fe(II) oxidation and the resulting Fe(III) phases have not been directly evaluated in complex soils or sediments with a mixture of phyllosilicates, Fe/Al oxides and a variety of organic compounds.
In this study, we sought to elucidate the individual roles of native soil minerals and native solid-phase OM in the Fe(II) oxidation process in soils. We hypothesized that Fe oxides would be a major catalyst for Fe(II) oxidation rates and would provide templates for crystalline Fe mineral formation, whereas soil OM would reduce oxidation rates and also result in a greater abundance of short-range-ordered (SRO) Fe(III) minerals. To test this, we treated soils to remove (a) OM, (b) Fe-oxides or (c) both, and then we investigated Fe(II) oxidation kinetics and the resulting de novo Fe(III) solids in both untreated and treated soils. Characterizing the newly formed Fe(III) phases is challenging because it is difficult to distinguish de novo Fe(III) phases from native soil Fe substrates using many spectroscopy techniques. To overcome this, we leveraged the isotope specificity of 57Fe Mössbauer spectroscopy to distinguish the isotopically labeled 57Fe(II) oxidation products from the native soil Fe (the 2% 57Fe in the native soil was corrected for using control spectra). These techniques allowed us to determine Fe oxidation states, the relative abundances, and the crystallinity of native and de novo Fe mineral phases.
Section snippets
Soil sampling
Soils for this study were collected from a cultivated site in the Calhoun Critical Zone Observatory (CCZO) in Union County, South Carolina, USA, and an upland valley site in the Bisley Research Watersheds of the Luquillo Experimental Forest of the Luquillo Critical Zone Observatory (LCZO) in Puerto Rico, USA, respectively. CCZO and LCZO soils are classified as Ultisols derived from granitic-gneiss and volcanic parent material with quartz diorite intrusions, respectively (Beinroth, 1982, Frizano
The native Fe phases in soils identified by Mössbauer spectroscopy
According to Mössbauer analysis, in all untreated soils, Fe-oxides comprised 80 – 85% of total Fe, with phyllosilicates/OM-bound Fe(III) accounting for an additional 10 – 12% of total Fe (Figs. 1a, A2 and A4; Tables A2, A4 and A5). Fe(II) was a minor component of LCZO topsoil (5% of total Fe) and was undetectable in both the CCZO topsoil and subsoil (Fig. 1a). The concentration of total Fe oxides in soils followed the order: CCZO subsoil (1061 mmol kg−1) > LCZO topsoil (973 mmol kg−1) ≫ CCZO
Native solid-phase OM retards Fe(II) oxidation; native Fe-oxides accelerate Fe(II) oxidation
Our results show that OM removal can accelerate the oxidation of Fe(II) in soils (Fig. 3; Table 1), indicating that native solid-phase OM retards Fe(II) oxidation rates in soils. In aqueous systems, previous studies have shown that complexation of Fe by dissolved organic ligands often alters Fe(II) oxidation kinetics—either accelerating or retarding the oxidation rate—based on the characteristics of Fe-binding organic ligands (Santana-Casiano et al., 2000, Santana-Casiano et al., 2004, Rose and
Conclusions
The results of this study indicate that, in addition to physiochemical conditions (pH, O2 concentration, etc.), native solid phases (especially Fe minerals and SOM content) will significantly affect the mobility of Fe(II) and the evolution of secondary Fe minerals in soils (Fig. 8). Our results reveal that native Fe-oxides play an outsized role in catalyzing Fe(II) oxidation and directing the de novo Fe mineral composition and crystallinity to resemble the parent minerals. We also find that the
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.
Acknowledgements
Gratitude is expressed to the National Natural Science Foundation of China (41907013) and the US National Science Foundation (EAR-1331841, EAR-1331846, EAR-1451508 and DEB-1457761) for financial support of the research.
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