skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Metallomics
DOI:https://doi.org/10.1039/c8mt00252e· OSTI ID:1507754
ORCiD logo [1];  [2];  [3];  [4]; ORCiD logo [4];  [4]; ORCiD logo [2]
  1. 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
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
  3. Oregon State Univ., Corvallis, OR (United States). College of Earth, Ocean, Atmospheric Sciences
  4. 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.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1507754
Alternate ID(s):
OSTI ID: 1482132
Report Number(s):
PNNL-SA-139283
Journal Information:
Metallomics, Vol. 11, Issue 1; ISSN 1756-5901
Publisher:
Royal Society of ChemistryCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 16 works
Citation information provided by
Web of Science

References (44)

Review on iron availability in soil: interaction of Fe minerals, plants, and microbes journal November 2013
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes journal June 2016
Current Review Siderophores in Microbial Interactions on Plant Surfaces journal January 1991
21 Tesla Fourier Transform Ion Cyclotron Resonance Mass Spectrometer Greatly Expands Mass Spectrometry Toolbox journal October 2016
The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake journal January 2015
Speciation of 2′-deoxymugineic acid–metal complexes in top soil extracts by multi-modal stationary phase LC-ICP-MS journal January 2015
Collision-induced dissociation of three groups of hydroxamate siderophores: ferrioxamines, ferrichromes and coprogens/fusigens journal July 2008
Acyl peptidic siderophores: structures, biosyntheses and post-assembly modifications journal February 2015
Ferric-Pyoverdine Recognition by Fpv Outer Membrane Proteins of Pseudomonas protegens Pf-5 journal December 2012
Mass spectral molecular networking of living microbial colonies journal May 2012
The Heterologous Siderophores Ferrioxamine B and Ferrichrome Activate Signaling Pathways in Pseudomonas aeruginosa journal February 2006
The effect of soil horizon and mineral type on the distribution of siderophores in soil journal April 2014
Siderophores in forest soil solution journal November 2004
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities journal September 2017
Modeling organic iron-binding ligands in a three-dimensional biogeochemical ocean model journal July 2015
An evolutionary mechanism for diversity in siderophore-producing bacteria: Siderophore diversity journal December 2011
Enterobactin: An archetype for microbial iron transport journal March 2003
An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS journal January 2015
Bacillibactin-Mediated Iron Transport in Bacillus s ubtilis 1 journal January 2006
Unambiguous identification and discovery of bacterial siderophores by direct injection 21 Tesla Fourier transform ion cyclotron resonance mass spectrometry journal January 2017
Occurrence of hydroxamate siderophore iron chelators in soils journal October 1980
Chemistry and biology of siderophores journal January 2010
Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils journal May 2018
Iron: Nutritious, Noxious, and Not Readily Available journal March 1994
Characterization of ‘Schizokinen’; a dihydroxamate-type siderophore produced by Rhizobium leguminosarum IARI 917 journal June 2006
Structure of schizokinen, An iron-transport compound from Bacillus megaterium journal December 1971
Collect reliable data on embryo selection journal November 2017
SIRIUS: decomposing isotope patterns for metabolite identification† journal November 2008
Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture journal June 2013
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal March 2012
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
Searching molecular structure databases with tandem mass spectra using CSI:FingerID journal September 2015
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 journal March 2014
Microbial Iron Acquisition: Marine and Terrestrial Siderophores journal October 2009
Complete Sequence of Virulence Plasmid pJM1 from the Marine Fish Pathogen Vibrio anguillarum Strain 775 journal September 2003
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 journal July 2015
The evolution of gene collectives: How natural selection drives chemical innovation journal January 2008
Metallophore mapping in complex matrices by metal isotope coded profiling of organic ligands journal January 2014
Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean journal December 2016
Isolation of the Siderophore Schizokinen from Soil of Rice Fields journal January 1983
Two Genomic Regions Involved in Catechol Siderophore Production by Erwinia carotovora journal January 1994
Siderophores in forest soil solution journal January 2005
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities text January 2017
Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities text January 2017

Cited By (3)

Metallophore profiling of nitrogen-fixing Frankia spp. to understand metal management in the rhizosphere of actinorhizal plants journal January 2019
Metallophores associated with Trichodesmium erythraeum colonies from the Gulf of Aqaba journal January 2019
Microbial Competition in the Subpolar Southern Ocean: An Fe–C Co-limitation Experiment journal January 2020

Similar Records

Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils
Journal Article · Tue May 01 00:00:00 EDT 2018 · Soil Biology and Biochemistry · OSTI ID:1507754

Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils
Journal Article · Tue May 01 00:00:00 EDT 2018 · Soil Biology and Biochemistry · OSTI ID:1507754

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 · OSTI ID:1507754