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

Boiteau, Rene M.; Shaw, Jared B.; Pasa-Tolic, Ljiljana; Koppenaal, David W.; Jansson, Janet K.

doi:10.1016/j.soilbio.2018.02.018

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

Journal Article · Thu Mar 08 00:00:00 EST 2018 · Soil Biology and Biochemistry

DOI:https://doi.org/10.1016/j.soilbio.2018.02.018· OSTI ID:1427526

^[1]; Shaw, Jared B. ^[1]; Pasa-Tolic, Ljiljana ^[1]; Koppenaal, David W. ^[1]; Jansson, Janet K. ^[2]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Earth and Biological Sciences Directorate

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 metallophores within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrices. 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) of soils from native tallgrass prairies in Kansas and Iowa. Both plant and fungal metallophores were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant Fe acquisition and homeostasis, including mugineic acids, deoxymugineic acid, nicotianamine, and hydroxynicotianamines, dominated the speciation of divalent metals such as Ni, Cu, and Zn (2–90 pmol/g soil). In contrast, the fungal siderophore ferricrocin was specific for trivalent Fe (7–32 pmol/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. In conclusion, small structural modifications result in significant differences in metal ligand selectivity, and likely impact metal uptake within the rhizosphere of grassland soils.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830; 49644

OSTI ID:: 1427526

Alternate ID(s):: OSTI ID: 1548618

Report Number(s):: PNNL-SA-128577; PII: S0038071718300671

Journal Information:: Soil Biology and Biochemistry, Vol. 120, Issue C; ISSN 0038-0717

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 22 works

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References (60)

Ecology of siderophores with special reference to the fungi Winkelmann, Günther BioMetals, Vol. 20, Issue 3-4 https://doi.org/10.1007/s10534-006-9076-1	journal	January 2007
Siderophores and the Dissolution of Iron-Bearing Minerals in Marine Systems Kraemer, S. M. Reviews in Mineralogy and Geochemistry, Vol. 59, Issue 1 https://doi.org/10.2138/rmg.2005.59.4	journal	January 2005
A review of recent trends in electrospray ionisation–mass spectrometry for the analysis of metal–organic ligand complexes Keith-Roach, Miranda J. Analytica Chimica Acta, Vol. 678, Issue 2 https://doi.org/10.1016/j.aca.2010.08.023	journal	September 2010
Ferricrocin functions as the main intracellular iron-storage compound in mycelia ofNeurospora crassa Matzanke, Berthold F.; Bill, Eckard; Trautwein, Alfred X. Biology of Metals, Vol. 1, Issue 1 https://doi.org/10.1007/BF01128013	journal	January 1988
Retention of phytosiderophores by the soil solid phase – adsorption and desorption Walter, M.; Oburger, E.; Schindlegger, Y. Plant and Soil, Vol. 404, Issue 1-2 https://doi.org/10.1007/s11104-016-2800-x	journal	February 2016
Geochemical Processes Constraining Iron Uptake in Strategy II Fe Acquisition Schenkeveld, W. D. C.; Schindlegger, Y.; Oburger, E. Environmental Science & Technology, Vol. 48, Issue 21 https://doi.org/10.1021/es5031728	journal	October 2014
Siderophores in environmental research: roles and applications: Siderophores in environmental research Ahmed, E.; Holmström, S. J. M. Microbial Biotechnology, Vol. 7, Issue 3 https://doi.org/10.1111/1751-7915.12117	journal	February 2014
Root exudation of phytosiderophores from soil‐grown wheat Oburger, Eva; Gruber, Barbara; Schindlegger, Yvonne New Phytologist, Vol. 203, Issue 4 https://doi.org/10.1111/nph.12868	journal	June 2014
Structural biology of bacterial iron uptake Krewulak, Karla D.; Vogel, Hans J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 9 https://doi.org/10.1016/j.bbamem.2007.07.026	journal	September 2008
Competition between micro‐organisms and roots of barley and sorghum for iron accumulated in the root apoplasm WirÉN, Nicolaus Von; RÖMheld, Volker; Shioiri, Takayuki New Phytologist, Vol. 130, Issue 4 https://doi.org/10.1111/j.1469-8137.1995.tb04328.x	journal	August 1995
Molecular aspects of Cu, Fe and Zn homeostasis in plants Grotz, Natasha; Guerinot, Mary Lou Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 7 https://doi.org/10.1016/j.bbamcr.2006.05.014	journal	July 2006
An angiotensin-I converting enzyme inhibitor from buckwheat (Fagopyrum esculentum Moench) flour Aoyagi, Yasuo Phytochemistry, Vol. 67, Issue 6 https://doi.org/10.1016/j.phytochem.2005.12.022	journal	March 2006
Relationships between Soybean Yield, Soil pH, and Soil Carbonate Concentration Rogovska, Natalia P.; Blackmer, Alfred M.; Mallarino, Antonio P. Soil Science Society of America Journal, Vol. 71, Issue 4 https://doi.org/10.2136/sssaj2006.0235	journal	July 2007
Siderophores in forest soil solution Holmstr�m, Sara J. M.; Lundstr�m, Ulla S.; Finlay, Roger D. Biogeochemistry, Vol. 71, Issue 2 https://doi.org/10.1007/s10533-004-9915-5	journal	November 2004
Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes Lemanceau, Philippe; Bauer, Petra; Kraemer, Stephan Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-009-0039-5	journal	June 2009
Mining iron: Iron uptake and transport in plants Kim, Sun A.; Guerinot, Mary Lou FEBS Letters, Vol. 581, Issue 12 https://doi.org/10.1016/j.febslet.2007.04.043	journal	April 2007
An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS Boiteau, Rene M.; Repeta, Daniel J. Metallomics, Vol. 7, Issue 5 https://doi.org/10.1039/C5MT00005J	journal	January 2015
Siderophore Utilization by Bradyrhizobium japonicum Plessner, Ora; Klapatch, Taryn; Guerinot, Mary Lou Applied and Environmental Microbiology, Vol. 59, Issue 5 https://doi.org/10.1128/AEM.59.5.1688-1690.1993	journal	May 1993
Detection and identification of ferricrocin produced by ectendomycorrhizal fungi in the genusWilcoxina Prabhu, Vikram; Biolchini, Peter F.; Boyer, Gregory L. BioMetals, Vol. 9, Issue 3 https://doi.org/10.1007/BF00817920	journal	July 1996
Synthesis and properties of different metal complexes of the siderophore desferriferricrocin Zou, Guozhang; Boyer, Gregory L. BioMetals, Vol. 18, Issue 1 https://doi.org/10.1007/s10534-004-5786-4	journal	February 2005
An Extracellular Siderophore Is Required to Maintain the Mutualistic Interaction of Epichloë festucae with Lolium perenne Johnson, Linda J.; Koulman, Albert; Christensen, Michael PLoS Pathogens, Vol. 9, Issue 5 https://doi.org/10.1371/journal.ppat.1003332	journal	May 2013
An Iron Uptake Operon Required for Proper Nodule Development in the Bradyrhizobium japonicum -Soybean Symbiosis Benson, Heather P.; Boncompagni, Eric; Guerinot, Mary Lou Molecular Plant-Microbe Interactions®, Vol. 18, Issue 9 https://doi.org/10.1094/MPMI-18-0950	journal	September 2005
A cross-platform toolkit for mass spectrometry and proteomics Chambers, Matthew C.; Maclean, Brendan; Burke, Robert Nature Biotechnology, Vol. 30, Issue 10 https://doi.org/10.1038/nbt.2377	journal	October 2012
Detection of Iron Ligands in Seawater and Marine Cyanobacteria Cultures by High-Performance Liquid Chromatography–Inductively Coupled Plasma-Mass Spectrometry Boiteau, Rene M.; Fitzsimmons, Jessica N.; Repeta, Daniel J. Analytical Chemistry, Vol. 85, Issue 9 https://doi.org/10.1021/ac3034568	journal	April 2013
Microbial Iron Acquisition: Marine and Terrestrial Siderophores Sandy, Moriah; Butler, Alison Chemical Reviews, Vol. 109, Issue 10 https://doi.org/10.1021/cr9002787	journal	October 2009
Vertical distribution of fungal communities in tallgrass prairie soil Jumpponen, Ari; Jones, Kenneth L.; Blair, John Mycologia, Vol. 102, Issue 5 https://doi.org/10.3852/09-316	journal	September 2010
Review on iron availability in soil: interaction of Fe minerals, plants, and microbes Colombo, Claudio; Palumbo, Giuseppe; He, Ji-Zheng Journal of Soils and Sediments, Vol. 14, Issue 3 https://doi.org/10.1007/s11368-013-0814-z	journal	November 2013
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes White, Richard Allen; Bottos, Eric M.; Roy Chowdhury, Taniya mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00045-16	journal	June 2016
Green Asparagus ( Asparagus officinalis ) Prevented Hypertension by an Inhibitory Effect on Angiotensin-Converting Enzyme Activity in the Kidney of Spontaneously Hypertensive Rats Sanae, Matsuda; Yasuo, Aoyagi Journal of Agricultural and Food Chemistry, Vol. 61, Issue 23 https://doi.org/10.1021/jf3041066	journal	May 2013
The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake Harrington, James M.; Duckworth, Owen W.; Haselwandter, Kurt BioMetals, Vol. 28, Issue 3 https://doi.org/10.1007/s10534-015-9821-4	journal	January 2015
Iron utilization and metabolism in plants Briat, Jean-François; Curie, Catherine; Gaymard, Frédéric Current Opinion in Plant Biology, Vol. 10, Issue 3 https://doi.org/10.1016/j.pbi.2007.04.003	journal	June 2007
Trace metal transport by marine microorganisms: implications of metal coordination kinetics Hudson, Robert J. M.; Morel, François M. M. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 40, Issue 1 https://doi.org/10.1016/0967-0637(93)90057-A	journal	January 1993
Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores R�mheld, V.; Marschner, H. Plant and Soil, Vol. 123, Issue 2 https://doi.org/10.1007/BF00011260	journal	April 1990
The effect of soil horizon and mineral type on the distribution of siderophores in soil Ahmed, Engy; Holmström, Sara J. M. Geochimica et Cosmochimica Acta, Vol. 131 https://doi.org/10.1016/j.gca.2014.01.031	journal	April 2014
The Ferrichrome Uptake Pathway in Pseudomonas aeruginosa Involves an Iron Release Mechanism with Acylation of the Siderophore and Recycling of the Modified Desferrichrome Hannauer, M.; Barda, Y.; Mislin, G. L. A. Journal of Bacteriology, Vol. 192, Issue 5 https://doi.org/10.1128/JB.01539-09	journal	January 2010
Nitrogen fertilization increases diversity and productivity of prairie communities used for bioenergy Jarchow, Meghann E.; Liebman, Matt GCB Bioenergy, Vol. 5, Issue 3 https://doi.org/10.1111/j.1757-1707.2012.01186.x	journal	June 2012
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis Outten, C. E. Science, Vol. 292, Issue 5526 https://doi.org/10.1126/science.1060331	journal	June 2001
Functional group and fertilization affect the composition and bioenergy yields of prairie plants Jarchow, Meghann E.; Liebman, Matt; Rawat, Vertika GCB Bioenergy, Vol. 4, Issue 6 https://doi.org/10.1111/j.1757-1707.2012.01184.x	journal	May 2012
Iron oxide dissolution and solubility in the presence of siderophores Kraemer, Stephan M. Aquatic Sciences - Research Across Boundaries, Vol. 66, Issue 1 https://doi.org/10.1007/s00027-003-0690-5	journal	March 2004
Tallgrass prairie soil fungal communities are resilient to climate change Jumpponen, Ari; Jones, Kenneth L. Fungal Ecology, Vol. 10 https://doi.org/10.1016/j.funeco.2013.11.003	journal	August 2014
Coordination chemistry of microbial iron transport compounds. 24. Characterization of coprogen and ferricrocin, two ferric hydroxamate siderophores Wong, Geoffrey B.; Kappel, Mary J.; Raymond, Kenneth N. Journal of the American Chemical Society, Vol. 105, Issue 4 https://doi.org/10.1021/ja00342a027	journal	February 1983
Quantification of Hydroxamate Siderophores in Soil Solutions of Podzolic Soil Profiles in Sweden Essén, Sofia A.; Bylund, Dan; Holmström, Sara J. M. BioMetals, Vol. 19, Issue 3 https://doi.org/10.1007/s10534-005-8418-8	journal	June 2006
Iron Uptake and Transport in Plants: The Good, the Bad, and the Ionome Morrissey, Joe; Guerinot, Mary Lou Chemical Reviews, Vol. 109, Issue 10 https://doi.org/10.1021/cr900112r	journal	October 2009
Root-Secreted Nicotianamine from Arabidopsis halleri Facilitates Zinc Hypertolerance by Regulating Zinc Bioavailability Tsednee, M.; Yang, S. -C.; Lee, D. -C. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.241224	journal	August 2014
Hydroxylated Phytosiderophore Species Possess an Enhanced Chelate Stability and Affinity for Iron(III) von Wirén, Nicolaus; Khodr, Hicham; Hider, Robert C. Plant Physiology, Vol. 124, Issue 3 https://doi.org/10.1104/pp.124.3.1149	journal	November 2000
Chemistry and biology of siderophores Hider, Robert C.; Kong, Xiaole Natural Product Reports, Vol. 27, Issue 5 https://doi.org/10.1039/b906679a	journal	January 2010
Sustainable bioenergy production from marginal lands in the US Midwest Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong Nature, Vol. 493, Issue 7433 https://doi.org/10.1038/nature11811	journal	January 2013
ZmYS1 Functions as a Proton-coupled Symporter for Phytosiderophore- and Nicotianamine-chelated Metals Schaaf, Gabriel; Ludewig, Uwe; Erenoglu, Bülent E. Journal of Biological Chemistry, Vol. 279, Issue 10 https://doi.org/10.1074/jbc.M311799200	journal	March 2004
Experimental considerations in metal mobilization from soil by chelating ligands: The influence of soil-solution ratio and pre-equilibration – A case study on Fe acquisition by phytosiderophores Schenkeveld, W. D. C.; Kimber, R. L.; Walter, M. Science of The Total Environment, Vol. 579 https://doi.org/10.1016/j.scitotenv.2016.11.168	journal	February 2017
Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake Curie, Catherine; Panaviene, Zivile; Loulergue, Clarisse Nature, Vol. 409, Issue 6818 https://doi.org/10.1038/35053080	journal	January 2001
Trace metal levels in edible wild fungi Severoglu, Z.; Sumer, S.; Yalcin, B. International Journal of Environmental Science and Technology, Vol. 10, Issue 2 https://doi.org/10.1007/s13762-012-0139-2	journal	December 2012
Inventory of metal complexes circulating in plant fluids: a reliable method based on HPLC coupled with dual elemental and high‐resolution molecular mass spectrometric detection Flis, Paulina; Ouerdane, Laurent; Grillet, Louis New Phytologist, Vol. 211, Issue 3 https://doi.org/10.1111/nph.13964	journal	April 2016
Acquisition, Transport, and Storage of Iron by Pathogenic Fungi Howard, Dexter H. Clinical Microbiology Reviews, Vol. 12, Issue 3 https://doi.org/10.1128/CMR.12.3.394	journal	July 1999
Kinetic studies on the specificity of chelate-iron uptake in Aspergillus Wiebe, C.; Winkelmann, G. Journal of Bacteriology, Vol. 123, Issue 3 https://doi.org/10.1128/JB.123.3.837-842.1975	journal	September 1975
Stabilities of Metal Complexes of Mugineic Acids and Their Specific Affinities for Iron(III) Murakami, Tasuku; Ise, Kunio; Hayakawa, Minato Chemistry Letters, Vol. 18, Issue 12 https://doi.org/10.1246/cl.1989.2137	journal	December 1989
Equilibrium and kinetic modelling of the dynamic rhizosphere Schenkeveld, W. D. C.; Kraemer, S. M. Plant and Soil, Vol. 386, Issue 1-2 https://doi.org/10.1007/s11104-014-2318-z	journal	December 2014
A specific transporter for iron(III)-phytosiderophore in barley roots Murata, Yoshiko; Ma, Jian Feng; Yamaji, Naoki The Plant Journal, Vol. 46, Issue 4 https://doi.org/10.1111/j.1365-313X.2006.02714.x	journal	May 2006
Facing the challenges of Cu, Fe and Zn homeostasis in plants Palmer, Christine M.; Guerinot, Mary Lou Nature Chemical Biology, Vol. 5, Issue 5 https://doi.org/10.1038/nchembio.166	journal	April 2009
Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean Boiteau, Rene M.; Mende, Daniel R.; Hawco, Nicholas J. Proceedings of the National Academy of Sciences, Vol. 113, Issue 50 https://doi.org/10.1073/pnas.1608594113	journal	December 2016
Fungal siderophore metabolism with a focus on Aspergillus fumigatus Haas, Hubertus Nat. Prod. Rep., Vol. 31, Issue 10 https://doi.org/10.1039/C4NP00071D	journal	January 2014

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59 BASIC BIOLOGICAL SCIENCES
Phytosiderophores
Hydroxamates
Metal exchange
High resolution mass spectrometry
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Title: Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils

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Cited By (4)

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