Calcareous organic matter coatings sequester siderophores in alkaline soils

Rene M. Boiteau; Ravi Kukkadapu; John B. Cliff; Chuck R. Smallwood; Libor Kovarik; Mark G. Wirth; Mark H. Engelhard; Tamas Varga; Alice Dohnalkova; Daniel E. Perea; Thomas Wietsma; James J. Moran; Kirsten S. Hofmockel

doi:10.1016/j.scitotenv.2020.138250

Calcareous organic matter coatings sequester siderophores in alkaline soils

Rene M. Boiteau, Ravi Kukkadapu, John B. Cliff, Chuck R. Smallwood, Libor Kovarik, Mark G. Wirth, Mark H. Engelhard, Tamas Varga, Alice Dohnalkova, Daniel E. Perea, Thomas Wietsma, James J. Moran, Kirsten S. Hofmockel

Research output: Contribution to journal › Article › peer-review

19 Scopus citations

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.

Original language	English
Article number	138250
Journal	Science of the Total Environment
Volume	724
DOIs	https://doi.org/10.1016/j.scitotenv.2020.138250
State	Published - Jul 1 2020
Externally published	Yes

Funding

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 DE-AC05-76RLO1830.

Funders	Funder number
U.S. Department of Energy
Battelle	DE-AC05-76RLO1830
Battelle
Biological and Environmental Research	LDRD 204495, EMSL-UP-50447
Biological and Environmental Research
Pacific Northwest National Laboratory

Keywords

Adsorption
Alkaline soil
Nanoscale
Organic-mineral interactions
Siderophores

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10.1016/j.scitotenv.2020.138250

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Boiteau, R. M., Kukkadapu, R., Cliff, J. B., Smallwood, C. R., Kovarik, L., Wirth, M. G., Engelhard, M. H., Varga, T., Dohnalkova, A., Perea, D. E., Wietsma, T., Moran, J. J., & Hofmockel, K. S. (2020). Calcareous organic matter coatings sequester siderophores in alkaline soils. Science of the Total Environment, 724, Article 138250. https://doi.org/10.1016/j.scitotenv.2020.138250

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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-M{\"o}ssbauer, 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.",

keywords = "Adsorption, Alkaline soil, Nanoscale, Organic-mineral interactions, Siderophores",

author = "Boiteau, {Rene M.} and Ravi Kukkadapu and Cliff, {John B.} and Smallwood, {Chuck R.} and Libor Kovarik and Wirth, {Mark G.} and Engelhard, {Mark H.} and Tamas Varga and Alice Dohnalkova and Perea, {Daniel E.} and Thomas Wietsma and Moran, {James J.} and Hofmockel, {Kirsten S.}",

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T1 - Calcareous organic matter coatings sequester siderophores in alkaline soils

AU - Boiteau, Rene M.

AU - Kukkadapu, Ravi

AU - Cliff, John B.

AU - Smallwood, Chuck R.

AU - Kovarik, Libor

AU - Wirth, Mark G.

AU - Engelhard, Mark H.

AU - Varga, Tamas

AU - Dohnalkova, Alice

AU - Perea, Daniel E.

AU - Wietsma, Thomas

AU - Moran, James J.

AU - Hofmockel, Kirsten S.

PY - 2020/7/1

Y1 - 2020/7/1

N2 - 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.

AB - 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.

KW - Adsorption

KW - Alkaline soil

KW - Nanoscale

KW - Organic-mineral interactions

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ER -

Calcareous organic matter coatings sequester siderophores in alkaline soils

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