Calcareous organic matter coatings sequester siderophores in alkaline soils

https://doi.org/10.1016/j.scitotenv.2020.138250Get rights and content

Highlights

  • Most natural organic carbon associated with Ca-rich coatings in an alkaline soil

  • Larger more hydrophilic siderophores exhibited greater affinity to soil particles.

  • Siderophores associated with organic carbon coatings rather than to bare mineral

  • Cation bridging of organic molecules was a major dominant stabilization mechanism.

Abstract

Although most studies of organic matter (OM) stabilization in soils have focused on adsorption to aluminosilicate and iron-oxide minerals due to their strong interactions with organic nucleophiles, stabilization within alkaline soils has been empirically correlated with exchangeable Ca. Yet the extent of competing processes within natural soils remains unclear because of inadequate characterization of soil mineralogy and OM distribution within the soil in relation to minerals, particularly in C poor alkaline soils. In this study, we employed bulk and surface-sensitive spectroscopic methods including X-ray diffraction, 57Fe-Mössbauer, and X-ray photoemission spectroscopy (XPS), and transmission electron microscopy (TEM) methods to investigate the minerology and soil organic C and N distribution on individual fine particles within an alkaline soil. Microscopy and XPS analyses demonstrated preferential sorption of Ca-containing OM onto surfaces of Fe-oxides and calcite. This result was unexpected given that the bulk combined amounts of quartz and Fe-containing feldspars of the soil constitute ~90% of total minerals and the surface atomic composition was largely Fe and Al (>10% combined) compared to Ca (4.2%). Soil sorption experiments were conducted with two siderophores, pyoverdine and enterobactin, to evaluate the adsorption of organic molecules with functional groups that strongly and preferentially bind Fe. A greater fraction of pyoverdine was adsorbed compared to enterobactin, which is smaller, less polar, and has a lower aqueous solubility. Using NanoSIMS to map the distribution of isotopically-labeled siderophores, we observed correlations with Ca and Fe, along with strong isotopic dilution with native C, indicating associations with OM coatings rather than with bare mineral surfaces. We propose a mechanism of adsorption by which organics aggregate within alkaline soils via cation bridging, favoring the stabilization of larger molecules with a greater number of nucleophilic functional groups.

Introduction

Organic compound-mineral associations control the stability of biomolecules and contaminants in soils as well as the size of soil organic matter (SOM) pools (Kaiser and Kalbitz, 2012; Kleber et al., 2015; Rasmussen et al., 2006). These interactions take various forms including direct inner and outer sphere complexes with Fe, Al, and Ca on the mineral surface or via cation bridging of organic functional groups (Kaiser and Guggenberger, 2000; Mikutta et al., 2007; Rowley et al., 2018). While the importance of specific interactions depends on soil texture, mineral type, and soil solution chemistry, it also depends on the functional groups comprising the organic matter (Chorover and Amistadi, 2001; Kennedy, 2002; Tipping, 1981a, Tipping, 1981b). Laboratory studies generally suggest preferential stabilization of components exhibiting stronger equilibrium constants of binding, in particular associations between carboxyl, or phenolic groups to Al- and Fe-oxide phases (Gu et al., 2008; Mikutta et al., 2014; Newcomb et al., 2017; Varadachari et al., 1998). These studies have primarily focused on acidic conditions, where adsorption of organic matter to metal oxides is maximized via associations with phenolic and carboxylic ligands (Gu et al., 2008). Yet in alkaline soils, strong correlations exist between exchangeable Ca concentrations and SOM content, implicating Ca binding mechanisms that occlude or adsorb OM (Bertrand et al., 2007; Clough and Skjemstad, 2000; Muneer and Oades, 1989; Rasmussen et al., 2018; Wuddivira and Camps-Roach, 2007). Thus, a major knowledge gap exists between laboratory-based expectations and empirical observations of factors that affect organic matter stabilization. This understanding is hindered by the complexity of mineral-organic associations within a heterogeneous mixture of fine particles.

Surface sensitive and nano-scale analyses of soils have recently shed light into the chemistry of SOM on individual soil particles (Chen et al., 2014; Garcia Arredondo et al., 2019; Mueller et al., 2012; Remusat et al., 2012; Vogel et al., 2014). X-ray photoemission spectroscopy (XPS) provides information on the elemental content and speciation of the outermost 2–10 nm surface layer, enabling the assessment of surface metal and carbon composition and the availability of sites for further substrate adsorption (Gerin et al., 2003; Woche et al., 2017; Yuan et al., 1998). Electron microscopy of soils further enables the characterization of individual particles at the nano-scale based on morphology, elemental composition, and electron diffraction patterns (Buatier et al., 2001; Chenu and Plante, 2006; Dohnalkova et al., 2017; Laird et al., 2008). While these tools are often employed independently, together with bulk 57Fe-specific Mössbauer spectroscopy and XRD analyses (Chen et al., 2017; Kaplan et al., 2016), they provide a means to evaluate the relative abundance of various mineral forms and also assess the extent to which organic matter associates preferentially with specific nano- or micro-particle phases in a natural soil setting. Here, we combined these techniques to determine whether organic matter in a natural alkaline soil associates primarily with Fe- and Al-bearing mineral surfaces, or another phase.

To identify structural features that play a role in organic sequestration under alkaline conditions, we then performed adsorption experiments with siderophores in the same alkaline soil. Siderophores are a large class of high-affinity iron chelating biomolecules. The chemical diversity of siderophores, their environmental relevance, and the ease of biologically synthesizing isotopically labeled forms make them appealing targets for studying how the structure and functionality of organic molecules influences mineral adsorption in soils. Hundreds of structurally distinct siderophores with a range of metal-binding functionalities, including catechols, hydroxamates, and carboxylic acids, have been identified to date (Hider and Kong, 2010). In alkaline soils and other environments where Fe solubility is poor, many organisms secrete siderophores to dissolve otherwise insoluble Fe and facilitate its transport across cell membranes (Sandy and Butler, 2009). Adsorption of siderophores to soil matrices reduces the efficiency of siderophore-mediated biological metal uptake (Harrington et al., 2015). While little is known about siderophore adsorption in alkaline soils, previous laboratory studies have demonstrated that siderophores adsorb to metal oxide surfaces by forming covalent bonds between catechol or hydroxamic acid moieties with surface cations (Upritchard et al., 2007, Upritchard et al., 2011). The stability constants of these siderophores generally rank Fe3+ > Al3+ > > Ca2+ (Athavale et al., 1966; Hider et al., 1982; Loomis and Raymond, 1991), implying that adsorption in soils may predominantly occur via associations with iron oxides and clay surfaces. However, siderophores can also adsorb to negative sites on humic substances or minerals via bridging with multivalent cations (Harrington et al., 2015; Higashi et al., 1998). Understanding the adsorption mechanisms of siderophores with different structures in alkaline soils may thus provide insight into the chemical characteristics that govern SOM adsorption more broadly.

To investigate sequestration mechanism in soils, we generated 13C and 15N isotopically-labeled siderophores, spiked them into the characterized alkaline soil, and mapped their surface distribution by NanoSIMS to identify the composition of surfaces to which the siderophores adsorbed. Our study focused on two common soil bacteria derived siderophores, pyoverdine and enterobactin, which have been previously observed in microbial enrichments from alkaline soils (Boiteau et al., 2019). These compounds have similar peptidic structures but contain different functional groups that impart metal binding, and they are easily purified from laboratory cultures. Our results suggest that in an alkaline soil comprised mainly of aluminosilicates and Fe-oxides, organic matter can preferentially form Ca bridges rather than adsorb directly to the surfaces of oxide minerals. These findings provide a possible explanation for why exchangeable cation content may govern organic matter adsorption in alkaline soils.

Section snippets

Soil collection and spectroscopic analysis

Soil from the Warden soil series (coarse-silty, mixed, super active, mesic Xeric Haplocambid) at the Washington State University Irrigated Agriculture Research and Extension Center near Prosser, WA, USA was collected in October 2017 from the top 15 cm. Since large particles interfere with analysis by TEM and NanoSIMS, the soil was sieved through a 4 mm mesh to remove large particles and then further sieved through a 53 μm mesh to obtain the fine fraction used for subsequent analyses. The 1:1

Naturally occurring minerals and Ca-organic matter associations

The mineralogical composition of Warden soil was investigated by a combination of analytical, spectroscopic, and microscopic analyses. Elemental analysis indicated the bulk soil was rich in Si (20.9 wt%) and Al (6.9 wt%), with Fe (5.3 wt%) and Ca (3.4 wt%) present at lower abundances. Silicate and aluminosilicate minerals included quartz and feldspars (anorthite and albite), based on the presence of diagnostic XRD peaks (Fig. S1). Mass balance calculations based on the room temperature

CRediT authorship contribution statement

Rene M. Boiteau:Conceptualization, Methodology, Investigation, Writing - original draft, Visualization.Ravi Kukkadapu:Conceptualization, Methodology, Investigation, Writing - original draft, Visualization, Project administration, Funding acquisition.John B. Cliff:Methodology, Investigation, Visualization, Writing - review & editing.Chuck R. Smallwood:Conceptualization, Investigation, Writing - review & editing.Libor Kovarik:Investigation, Visualization, Writing - review & editing.Mark G. Wirth:

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.

Acknowledgments

This research was supported by the Department of Energy (DOE) Office of Biological and Environmental Research (BER) and was conducted at the Environmental Molecular Sciences Laboratory (EMSL), a DOE user facility, as a contribution of the EMSL Strategic Science Area under project (EMSL-UP-50447). R Boiteau was funded by the Linus Pauling Postdoctoral Fellowship LDRD 204495 from the Pacific Northwest National Lab (PNNL). PNNL is operated for the DOE by Battelle Memorial Institute under Contract

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