Distinct roles of pH and organic ligands in the dissolution of goethite by cysteine

https://doi.org/10.1016/j.jes.2021.06.011Get rights and content

Highlights

  • The rate constant of Fe(II) release and generation correlated with cysteine.

  • A low pH thermodynamically enhanced electron transfer from cysteine to goethite.

  • Organic ligands only kinetically promoted release of the less available Fe(II).

  • Electron transfer from cysteine to goethite was via S-S complexation on goethite.

Abstract

Electron shuttles such cysteine play an important role in Fe cycle and its availability in soils, while the roles of pH and organic ligands in this process are poorly understood. Herein, the reductive dissolution process of goethite by cysteine were explored in the presence of organic ligands. Our results showed that cysteine exhibited a strong reactivity towards goethite – a typical iron minerals in paddy soils with a rate constant ranging from 0.01 to 0.1 hr−1. However, a large portion of Fe(II) appeared to be “structural species” retained on the surface. The decline of pH was favorable to generate more Fe(II) ions and enhancing tendency of Fe(II) release to solution. The decline of generation of Fe(II) by increasing pH was likely to be caused by a lower redox potential and the nature of cysteine pH-dependent adsorption towards goethite. Interestingly, the co-existence of oxalate and citrate ligands also enhanced the rate constant of Fe(II) release from 0.09 to 0.15 hr−1; nevertheless, they negligibly affected the overall generation of Fe(II) in opposition to the pH effect. Further spectroscopic evidence demonstrated that two molecules of cysteine could form disulfide bonds (S-S) to generate cystine through oxidative dehydration, and subsequently, inducing electron transfer from cysteine to the structural Fe(III) on goethite; meanwhile, those organic ligands act as Fe(II) “strippers”. The findings of this work provide new insights into the understanding of the different roles of pH and organic ligands on the generation and release of Fe induced by electron shuttles in soils.

Introduction

Iron (Fe) is one of the essential elements for the growth of plants and microorganisms on earth (Konhauser et al., 2011; Marschner, 1995). Despite the fact that the relative abundance of Fe in the earth's crust and soils is considerably high, the nature of the strong hydrolysis of Fe(III) to form Fe(III) oxyhydroxides results to a poor accessibilities by organisms/plants (Sparks, 2003; Sposito, 1994; Stumm and Lee, 1961). To tackle the deficiency of available Fe in soils, there are several strategies involved with organisms to promote the dissolution of iron oxides, including protons-promoted dissolution and ligands-promoted dissolution (Schenkeveld et al., 2016; Zinder et al., 1986). Previous studies have shown that organic ligands such as desferrioxamine B, citrate and oxalate, have high affinities towards Fe(III) oxyhydroxides through complexation with structural Fe(III) and turning to soluble ligand-Fe(III) complexes (Cervini-Silva and Sposito, 2002; Kraemer, 2004; Li et al., 2016; Schenkeveld et al., 2016; Suzuki et al., 1992; Urrutia et al., 1999). Such process is generally considered as the predominant path for Fe uptake by plants and microorganisms in the environment.

Recently, microbially induced electron transfer and redox processes have attracted increasingly interest due to their great impacts on the element cycles and the pollutant transformation (Li et al., 2015; Liu et al., 2020; Rui et al., 2013; Stams et al., 2006). Evidence suggests that the interaction between electroactive microorganisms and iron oxides is of particular importance in the Fe biogeochemical cycles. A few studies showed that small organic molecules (e.g., flavin, antraquinone-2,6-disulfonate and cysteine) excreted by microorganisms could act as electron shuttles to transfer electrons to the surface of iron oxides through surface complexes (Doong and Schink, 2002; Ma et al., 2015; Shi et al., 2016; Van der Zee and Cervantes, 2009; Xuan and Liang, 2017; Zhao et al., 2019). Accordingly, this becomes a key mechanism accelerating the electron transfer between microbes and minerals. Of these electron shuttles, cysteine containing a thiol structure (Doong and Schink, 2002; Giles et al., 2003) and three de-protonatable functional groups (i.e., -SH, -NH2 and -COOH) with pKa values of 1.71, 8.33 and 10.78 (Amirbahman et al., 1997; Salemi et al., 2009), respectively, exhibiting a great potential in complexing with Fe(III) oxyhydroxides under varying conditions. Considering the low redox potential of cysteine, this compound is likely to determine the Fe bioavailability in soils. However, such redox process may also relate with environmental conditions (e.g., pH), subsequently affecting the electron transfer process and the Fe bioavailability (e.g., Fe(II) generation and release). Meanwhile, the concomitant organic ligands such as citrate and oxalate by microorganisms or plants are also ubiquitous in soils, which have strong capability of complexing with Fe and possibly competing for the sites on the surface of iron oxides with cysteine (Elaine et al., 2017; Liu and Huang, 2003). All these scenarios may complicate this electron transferring process; however, the understanding of these effects on the bioavailability of Fe is largely scarce.

In this work, the interaction of three electron shuttles, namely cysteine, tryptophan and tyrosine on the surface of goethite – a typical Fe(III) oxyhydroxide widely presented in agricultural soils – was initially evaluated and the reductive dissolution of goethite by cysteine was systematically investigated under different conditions of solution pH and the presence of organic ligands, in terms of the generation and release of Fe(II). Subsequently, the adsorption and transformation of cysteine in the presence of goethite was analyzed. In addition, different effects of pH and organic ligands (i.e., citrate and oxalate) on the Fe(II) generation and release kinetics during the course of reductive dissolution of goethite were examined; and finally the underlying mechanisms were explored by spectroscopic and electrochemical techniques.

Section snippets

Chemicals

Iron nitrate nonahydrate (Fe(NO3)3•9H2O, 99.9%), potassium hydroxide (KOH, 85%), disodium hydrogen phosphate dodecahydrate (Na2HPO4•12H2O, 99%), sodium dihydrogen phosphate dihydrate (NaH2PO4•2H2O, 99%), 1,10-phenanthroline (C12H8N2•H2O, 99%), glycine (C2H5NO2, 99%), nitrilotriacetic acid (N(CH2COOH)3, 99%), oxalic acid dihydrate (C2H2O4•2H2O, 99%), and citric acid monohydrate (C6H8O7•H2O, 99%) were obtained from Sinopharm Chemical Reagent Co. Ltd., China. Morpholine ethanesulfonic acid (C6H13NO

Fe(II) generation and release kinetics

Prior to batch experiments, the structure and morphology of the prepared goethite were systematically characterized. As shown in Appendix A Fig. S1a, the XRD patterns of the as-prepared goethite exhibits typical three characteristic peaks at ~ 21.2°, ~ 33.2°, and ~ 36.6°, corresponding to the facets of (101), (301) and (100) of goethite (Hou et al., 2017). The SSA of the prepared goethite was found to be 98 m2/g (Appendix A Fig. S1b). The SEM image of the goethite showed a rod-like crystal

Conclusions

This study examined the effects of pH and organic ligands on the interaction of electron shuttle (i.e., cysteine) with goethite, which was highly related to the bioavailability of Fe in soils. Our results suggested that the rate constant kobs value notably increased linearly from 0.05 to 0.10 hr−1 with the increase of cysteine concentration from 0.1 to 1 mmol/L. More importantly, the different roles of pH and organic ligands (i.e., oxalate and citrate) in accelerating the Fe(II) release from

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Nos. 42077301; 21876161), and the National Key Research and Development Project of China (No. 2020YFC1808702), Guangdong Academy of Sciences’ Project (No. 2019GDASYL-0102006).

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