Changes in the structure of birnessite during siderophore-promoted dissolution: A time-resolved synchrotron X-ray diffraction study

We used time-resolved synchrotron X-ray diffraction to follow the complete dissolution of synthetic triclinic Na-birnessite as promoted by the trihydroxamate siderophore desferrioxamine B (DFOB). Many microorganisms employ siderophores to increase the availability of Fe, Mn, and other trace metals for metabolic processes. Our primary goal was to quantify the DFOB-assisted dissolution rate by direct, continuous observation of the solid phase. Our kinetic model indicates that the rate of dissolution is dependent on [DFOB] but not pH, and has a reaction order of 0.505 with a rate constant of 0.112 wt%birn min^{− 1}. The unit-cell dimensions of birnessite remained virtually constant within error throughout the dissolution process, showing only a 0.3% contraction along the c-axis. Despite the small changes in unit-cell volume, Rietveld analysis revealed that the occupancy of Mn within the octahedral sheets decreased from 100% to ~ 80%, presumably as the result of complexation of structural Mn^{3 +} with DFOB followed by extraction of Mn^{3 +} from the crystal structure. These observations suggest a critical lacunarity of ~ 20 mol% Mn for triclinic Na-birnessite, below which the structure is destabilized. Moreover, this study reveals that DFOB-promoted dissolution must operate by a different mechanism from that engaged when bacterial membrane fractions directly transfer electrons to birnessite crystals. We propose that crystal structure analysis of minerals undergoing dissimilatory metal reduction can elucidate metabolic pathways employed by microorganisms.