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

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

Research output: Contribution to journalArticlepeer-review

23 Scopus citations

Abstract

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. Here 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.

Original languageEnglish (US)
Pages (from-to)166-175
Number of pages10
JournalMetallomics
Volume11
Issue number1
DOIs
StatePublished - Jan 2019
Externally publishedYes

Bibliographical note

Funding Information:
We would like to thank Joseph Brown for bioinformatics assistance and Robert Starke for advice regarding microbial enrichment cultures. This research was supported by the U.S. Department of Energy Office of Biological and Environmental Research (BER) and is a contribution of the Scientific Focus Area ‘Phenotypic response of the soil microbiome to environmental perturbations’ (70880). R. Boiteau was funded by the Linus Pauling Postdoctoral Fellowship LDRD 204495 from the Pacific Northwest National Lab. This work was conducted at the Environmental Molecular Sciences Laboratory, a U.S. Department of Energy user facility, under project 49644. PNNL is operated for the DOE by Battelle Memorial Institute under Contract DE-AC05-76RLO1830.

Publisher Copyright:
© 2019 The Royal Society of Chemistry.

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