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Title: Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils

Abstract

Many elements are scarcely soluble in aqueous conditions found in high pH environments, such as calcareous grassland soils, unless complexed to strong binding organic ligands. To overcome this limitation, some plants and microbes produce chelators that solubilize micronutrient metals such as Fe, Ni, Cu, and Zn from mineral phases. These complexes are taken up by organisms via specific membrane receptors, thereby differentially impacting the bioavailability of these metals to the plant and microbial community. Although the importance of these chelation strategies for individual organisms has been well established, little is known about which pathways coexist within rhizosphere microbiomes or how they interact and compete for metal binding. Identifying these metallo-organic species within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrix. Herein, we employed recently developed liquid chromatography (LC) mass spectrometry (MS) methods to characterize the speciation of water-soluble dissolved trace elements (Fe, Ni, Cu, and Zn) from Kansas Prairie soil. Both plant and fungal chelators were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant iron acquisition and homeostasis, including mugineic acids, deoxymugineic acid, nicotianamine, and hydroxynicotianamine,more » dominated the speciation of divalent metals such as Ni, Cu, and Zn (2-57 pmol / g soil). In contrast, the fungal siderophore ferricrocine bound comparatively more trivalent Fe (9pmol / g soil). These results define biochemical pathways that underpin the regulation of metals in the grassland rhizosphere. They also raise new questions about the competition of these compounds for metal binding and their bioavailability to different members of the rhizosphere population. Even small structural differences result in significant differences in their environmental metal speciation, and likely impact metal uptake within the rhizosphere of calcareous soils.« less

Authors:
ORCiD logo; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1434844
Report Number(s):
PNNL-SA-128577
Journal ID: ISSN 0038-0717; 49644
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Soil Biology and Biochemistry; Journal Volume: 120; Journal Issue: C
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., and Jansson, Janet K.. Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils. United States: N. p., 2018. Web. doi:10.1016/j.soilbio.2018.02.018.
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., & Jansson, Janet K.. Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils. United States. doi:10.1016/j.soilbio.2018.02.018.
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., and Jansson, Janet K.. Tue . "Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils". United States. doi:10.1016/j.soilbio.2018.02.018.
@article{osti_1434844,
title = {Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils},
author = {Boiteau, Rene M. and Shaw, Jared B. and Pasa-Tolic, Ljiljana and Koppenaal, David W. and Jansson, Janet K.},
abstractNote = {Many elements are scarcely soluble in aqueous conditions found in high pH environments, such as calcareous grassland soils, unless complexed to strong binding organic ligands. To overcome this limitation, some plants and microbes produce chelators that solubilize micronutrient metals such as Fe, Ni, Cu, and Zn from mineral phases. These complexes are taken up by organisms via specific membrane receptors, thereby differentially impacting the bioavailability of these metals to the plant and microbial community. Although the importance of these chelation strategies for individual organisms has been well established, little is known about which pathways coexist within rhizosphere microbiomes or how they interact and compete for metal binding. Identifying these metallo-organic species within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrix. Herein, we employed recently developed liquid chromatography (LC) mass spectrometry (MS) methods to characterize the speciation of water-soluble dissolved trace elements (Fe, Ni, Cu, and Zn) from Kansas Prairie soil. Both plant and fungal chelators were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant iron acquisition and homeostasis, including mugineic acids, deoxymugineic acid, nicotianamine, and hydroxynicotianamine, dominated the speciation of divalent metals such as Ni, Cu, and Zn (2-57 pmol / g soil). In contrast, the fungal siderophore ferricrocine bound comparatively more trivalent Fe (9pmol / g soil). These results define biochemical pathways that underpin the regulation of metals in the grassland rhizosphere. They also raise new questions about the competition of these compounds for metal binding and their bioavailability to different members of the rhizosphere population. Even small structural differences result in significant differences in their environmental metal speciation, and likely impact metal uptake within the rhizosphere of calcareous soils.},
doi = {10.1016/j.soilbio.2018.02.018},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 120,
place = {United States},
year = {Tue May 01 00:00:00 EDT 2018},
month = {Tue May 01 00:00:00 EDT 2018}
}