Article pubs.acs.org/est
Aerobic Microbial Fe Acquisition from Ferrihydrite Nanoparticles: Effects of Crystalline Order, Siderophores, and Alginate K. M. Kuhn,† J. L. DuBois,‡ and P. A. Maurice*,† †
Department of Civil and Environmental Engineering and Earth Sciences, University of Notre Dame, 156 Fitzpatrick Hall, Notre Dame, Indiana 46556, United States ‡ Department of Chemistry and Biochemistry, Montana State University, 103 Chemistry and Biochemistry Building, Bozeman, Montana 59717, United States S Supporting Information *
ABSTRACT: This research compared the bioavailability of Fe associated with two forms of the hydrous Fe oxyhydroxide nanomineral ferrihydrite (Fh)the smaller (1−3 nm), less ordered 2-line (2L) phase and the slightly larger, (2−6 nm) more ordered 6-line (6L) phaseto the common aerobic soil bacterium Pseudomonas mendocina ymp. P. mendocina can acquire Fe from minerals using high-affinity Fe(III) binding ligands known as siderophores and a cellassociated metalloreductase that requires direct cell-mineral contact. Wild-type (WT) P. mendocina and a siderophore(−) mutant were used to monitor siderophore −related and −independent Fe acquisition from 2L and 6L Fh. Both WT and mutant strains acquired Fe from Fh, although Fe acquisition and growth were substantially greater on the 2L phase than on the 6L phase. In the absence of bacteria, copious quantities of the biofilm exopolysaccharide alginate slightly promoted dissolution of 2L and 6L Fh. In biotic experiments, added alginate slightly enhanced growth and Fe acquisition from 6L Fh but not from 2L Fh. Recent research has led to an emerging understanding that Fe-oxide nanoparticle structure, stability, and reactivity are highly sensitive to size at the nanoscale; this research emphasizes how subtle differences in nanoparticle size-related properties can also affect bioavailability.
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aggregated) and is thus a “nanomineral”.10 The poorly ordered 2-line (“less crystalline”, 2L) phase, where “line” refers to X-ray diffraction maxima,6 tends to occur as ∼2−4 nm nanoparticles; particles of the more ordered 6-line (6L) phase are slightly larger.11 The structure of Fh and how it may change with particle size or incorporation of impurities remain topics of much active research6,12,13 because of the nanomineral’s broad environmental importance. Rates of siderophore-mediated dissolution of hematite (αFe2O3)which has a higher crystalline order than Fh and does not contain structural waterincrease as nanoparticle size decreases.14 Hematite bioavailability to P. mendocina3 has been shown to increase as nanoparticle size decreases. We thus hypothesized that differences in 2L versus 6L Fh nanoparticles could also be important for Fe bioavailability. To test this hypothesis, a wild-type (WT) strain of P. mendocina and an engineered mutant (ΔpmhA) with a siderophore(−) phenotype were used to compare growth on 2L and 6L Fh in Felimited batch cultures. Both strains were appended with a molecular biosensor,15 which allowed for direct quantification of Fe deficiency sensed inside the cell. Previous work focused on differences in bioavailability of hematite particles
