Siderophore profiling of co-habitating soil bacteria by ultra-high resolution mass spectrometry

Boiteau, Rene M.; Fansler, Sarah J.; Farris, Yuliya; Shaw, Jared B.; Koppenaal, David W.; Pasa-Tolic, Ljiljana; Jansson, Janet K.

doi:10.1039/c8mt00252e

Siderophore profiling of co-habitating soil bacteria by ultra-high resolution mass spectrometry

Journal Article · Wed Nov 14 00:00:00 EST 2018 · Metallomics

DOI:https://doi.org/10.1039/c8mt00252e· OSTI ID:1507754

^[1]; Fansler, Sarah J. ^[2]; Farris, Yuliya ^[3]; Shaw, Jared B. ^[4]; ^[4]; Pasa-Tolic, Ljiljana ^[4]; ^[2]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.; Oregon State Univ., Corvallis, OR (United States). College of Earth, Ocean, Atmospheric Sciences
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
Oregon State Univ., Corvallis, OR (United States). College of Earth, Ocean, Atmospheric Sciences
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.

The chemical structure of organic molecules profoundly impacts their interactions with metal ions and mineral phases in soils. Understanding the sources and cycling of metal-chelating compounds is therefore essential for predicting the bioavailability and transport of metals throughout terrestrial environments. We investigate the molecular speciation of organic molecules that solubilize trace metals in calcareous soils from Eastern Washington. Ultra-high performance Fourier transform ion cyclotron resonance mass spectrometry at 21 Tesla enabled fast and confident detection and identification of metal chelators that are produced by microbes that inhabit these soils based on screening for features that match diagnostic metal isotope patterns. We compared two approaches, one based on direct infusion using the incorporation of a rare isotope to validate true iron-binding features, and another based on separation with liquid chromatography and detection of isotopologues with coherent elution profiles. While the isotopic exchange method requires significantly shorter analysis time, nearly twice as many features were observed with liquid chromatography mass spectrometry (LCMS), mostly due to the reduction in ion suppression where major features limit the sensitivity of minor features. In addition, LCMS enabled the collection of higher quality fragmentation spectra and facilitated feature identification. Siderophores belonging to four major classes were identified, including ferrioxamines, pseudobactins, enterobactins, and arthrobactins. Each of these siderophores likely derives from a unique member of the microbial community, and each possesses different chemical characteristics and uptake pathways, likely contributing to fierce competition for iron within these soils. Our results provide insight into the metabolic pathways by which microbes that co-inhabit calcareous soils compete for this essential micronutrient.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1507754

Alternate ID(s):: OSTI ID: 1482132

Report Number(s):: PNNL-SA--139283

Journal Information:: Metallomics, Journal Name: Metallomics Journal Issue: 1 Vol. 11; ISSN 1756-5901

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

References (45)

Accurate LC-ESI-MS/MS quantification of 2′-deoxymugineic acid in soil and root related samples employing porous graphitic carbon as stationary phase and a ¹³ C ₄ -labeled internal standard : Liquid Phase Separations Schindlegger, Yvonne; Oburger, Eva; Gruber, Barbara ELECTROPHORESIS, Vol. 35, Issue 9 https://doi.org/10.1002/elps.201300551	journal	March 2014
Collision-induced dissociation of three groups of hydroxamate siderophores: ferrioxamines, ferrichromes and coprogens/fusigens Mawji, Edward; Gledhill, Martha; Worsfold, Paul J. Rapid Communications in Mass Spectrometry, Vol. 22, Issue 14 https://doi.org/10.1002/rcm.3604	journal	July 2008
Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture Radzki, W.; Gutierrez Mañero, F. J.; Algar, E. Antonie van Leeuwenhoek, Vol. 104, Issue 3 https://doi.org/10.1007/s10482-013-9954-9	journal	June 2013
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
Siderophores in forest soil solution Holmström, Sara J. M.; Lundström, Ulla S.; Finlay, Roger D. Biogeochemistry, Vol. 71, Issue 2 https://doi.org/10.1007/s10533-005-0015-y	journal	January 2005
Characterization of ‘Schizokinen’; a dihydroxamate-type siderophore produced by Rhizobium leguminosarum IARI 917 Storey, E. P.; Boghozian, R.; Little, James L. BioMetals, Vol. 19, Issue 6 https://doi.org/10.1007/s10534-006-9001-7	journal	June 2006
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
Acyl peptidic siderophores: structures, biosyntheses and post-assembly modifications Kem, Michelle P.; Butler, Alison BioMetals, Vol. 28, Issue 3 https://doi.org/10.1007/s10534-015-9827-y	journal	February 2015
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
21 Tesla Fourier Transform Ion Cyclotron Resonance Mass Spectrometer Greatly Expands Mass Spectrometry Toolbox Shaw, Jared B.; Lin, Tzu-Yung; Leach, Franklin E. Journal of The American Society for Mass Spectrometry, Vol. 27, Issue 12 https://doi.org/10.1007/s13361-016-1507-9	journal	October 2016
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
Investigating the potential of solid-phase extraction and Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR-MS) for the isolation and identification of dissolved metal–organic complexes from natural waters Waska, Hannelore; Koschinsky, Andrea; Ruiz Chancho, Maria Jose Marine Chemistry, Vol. 173 https://doi.org/10.1016/j.marchem.2014.10.001	journal	July 2015
Modeling organic iron-binding ligands in a three-dimensional biogeochemical ocean model Völker, Christoph; Tagliabue, Alessandro Marine Chemistry, Vol. 173 https://doi.org/10.1016/j.marchem.2014.11.008	journal	July 2015
Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils Boiteau, Rene M.; Shaw, Jared B.; Pasa-Tolic, Ljiljana Soil Biology and Biochemistry, Vol. 120 https://doi.org/10.1016/j.soilbio.2018.02.018	journal	May 2018
Structure of schizokinen, An iron-transport compound from Bacillus megaterium Mullis, Kary B.; Pollack, J. R.; Neilands, J. B. Biochemistry, Vol. 10, Issue 26 https://doi.org/10.1021/bi00802a010	journal	December 1971
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
Identification of a Cluster of Genes that Directs Desferrioxamine Biosynthesis in Streptomyces c oelicolor M145 Barona-Gómez, Francisco; Wong, Ursula; Giannakopulos, Anastassios E. Journal of the American Chemical Society, Vol. 126, Issue 50 https://doi.org/10.1021/ja045774k	journal	December 2004
Bacillibactin-Mediated Iron Transport in Bacillus s ubtilis ¹ Dertz, Emily A.; Xu, Jide; Stintzi, Alain Journal of the American Chemical Society, Vol. 128, Issue 1 https://doi.org/10.1021/ja055898c	journal	January 2006
Occurrence of hydroxamate siderophore iron chelators in soils Powell, P. E.; Cline, G. R.; Reid, C. P. P. Nature, Vol. 287, Issue 5785 https://doi.org/10.1038/287833a0	journal	October 1980
Collect reliable data on embryo selection Thompson, Charis Nature, Vol. 551, Issue 7678 https://doi.org/10.1038/551033a	journal	November 2017
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities Butaitė, Elena; Baumgartner, Michael; Wyder, Stefan Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00509-4	journal	September 2017
Metallophore mapping in complex matrices by metal isotope coded profiling of organic ligands Deicke, Michael; Mohr, Jan Frieder; Bellenger, Jean-Philippe The Analyst, Vol. 139, Issue 23 https://doi.org/10.1039/C4AN01461H	journal	January 2014
Speciation of 2′-deoxymugineic acid–metal complexes in top soil extracts by multi-modal stationary phase LC-ICP-MS Schindlegger, Y.; Oburger, E.; Puschenreiter, M. Journal of Analytical Atomic Spectrometry, Vol. 30, Issue 6 https://doi.org/10.1039/C5JA00018A	journal	January 2015
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
Unambiguous identification and discovery of bacterial siderophores by direct injection 21 Tesla Fourier transform ion cyclotron resonance mass spectrometry Walker, Lawrence R.; Tfaily, Malak M.; Shaw, Jared B. Metallomics, Vol. 9, Issue 1 https://doi.org/10.1039/C6MT00201C	journal	January 2017
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
The long-overlooked enzymology of a nonribosomal peptide synthetase-independent pathway for virulence-conferring siderophore biosynthesis Oves-Costales, Daniel; Kadi, Nadia; Challis, Gregory L. Chemical Communications, Issue 43 https://doi.org/10.1039/b913092f	journal	January 2009
Enterobactin: An archetype for microbial iron transport Raymond, K. N.; Dertz, E. A.; Kim, S. S. Proceedings of the National Academy of Sciences, Vol. 100, Issue 7 https://doi.org/10.1073/pnas.0630018100	journal	March 2003
The evolution of gene collectives: How natural selection drives chemical innovation Fischbach, M. A.; Walsh, C. T.; Clardy, J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 12 https://doi.org/10.1073/pnas.0709132105	journal	January 2008
Mass spectral molecular networking of living microbial colonies Watrous, J.; Roach, P.; Alexandrov, T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 26 https://doi.org/10.1073/pnas.1203689109	journal	May 2012
Searching molecular structure databases with tandem mass spectra using CSI:FingerID Dührkop, Kai; Shen, Huibin; Meusel, Marvin Proceedings of the National Academy of Sciences, Vol. 112, Issue 41 https://doi.org/10.1073/pnas.1509788112	journal	September 2015
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
SIRIUS: decomposing isotope patterns for metabolite identification† Böcker, Sebastian; Letzel, Matthias C.; Lipták, Zsuzsanna Bioinformatics, Vol. 25, Issue 2 https://doi.org/10.1093/bioinformatics/btn603	journal	November 2008
Current Review Siderophores in Microbial Interactions on Plant Surfaces Loper, Joyce E. Molecular Plant-Microbe Interactions, Vol. 4, Issue 1 https://doi.org/10.1094/MPMI-4-005	journal	January 1991
Iron: Nutritious, Noxious, and Not Readily Available Guerinot, M. L.; Yi, Y. Plant Physiology, Vol. 104, Issue 3 https://doi.org/10.1104/pp.104.3.815	journal	March 1994
An evolutionary mechanism for diversity in siderophore-producing bacteria: Siderophore diversity Lee, William; van Baalen, Minus; Jansen, Vincent A. A. Ecology Letters, Vol. 15, Issue 2 https://doi.org/10.1111/j.1461-0248.2011.01717.x	journal	December 2011
Isolation of the Siderophore Schizokinen from Soil of Rice Fields Akers, Hugh A. Applied and Environmental Microbiology, Vol. 45, Issue 5 https://doi.org/10.1128/AEM.45.5.1704-1706.1983	journal	January 1983
Two Genomic Regions Involved in Catechol Siderophore Production by Erwinia carotovora Bull, Carolee T.; Ishimaru, Carol A.; Loper, Joyce E. Applied and Environmental Microbiology, Vol. 60, Issue 2 https://doi.org/10.1128/AEM.60.2.662-669.1994	journal	January 1994
Ferric-Pyoverdine Recognition by Fpv Outer Membrane Proteins of Pseudomonas protegens Pf-5 Hartney, S. L.; Mazurier, S.; Girard, M. K. Journal of Bacteriology, Vol. 195, Issue 4 https://doi.org/10.1128/JB.01639-12	journal	December 2012
Complete Sequence of Virulence Plasmid pJM1 from the Marine Fish Pathogen Vibrio anguillarum Strain 775 Di Lorenzo, Manuela; Stork, Michiel; Tolmasky, Marcelo E. Journal of Bacteriology, Vol. 185, Issue 19 https://doi.org/10.1128/JB.185.19.5822-5830.2003	journal	September 2003
The Heterologous Siderophores Ferrioxamine B and Ferrichrome Activate Signaling Pathways in Pseudomonas aeruginosa Llamas, M. A.; Sparrius, M.; Kloet, R. Journal of Bacteriology, Vol. 188, Issue 5 https://doi.org/10.1128/JB.188.5.1882-1891.2006	journal	February 2006
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
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities Butaitė, Elena; Baumgartner, Michael; Wyder, Stefan ETH Zurich https://doi.org/10.3929/ethz-b-000236935	text	January 2017
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities Butaitė, Elena; Baumgartner, Michael; Wyder, Stefan Nature Publishing Group https://doi.org/10.5167/uzh-144478	text	January 2017

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