Iron-oxo clusters biomineralizing on protein surfaces: structural analysis of Halobacterium salinarum DpsA in its low- and high-iron states.

The crystal structure of the Dps-like (Dps, DNA-protecting protein during starvation) ferritin protein DpsA from the halophile Halobacterium salinarum was determined with low endogenous iron content at 1.6-A resolution. The mechanism of iron uptake and storage was analyzed in this noncanonical ferritin by three high-resolution structures at successively increasing iron contents. In the high-iron state of the DpsA protein, up to 110 iron atoms were localized in the dodecameric protein complex. For ultimate iron storage, the archaeal ferritin shell comprises iron-binding sites for iron translocation, oxidation, and nucleation. Initial iron-protein interactions occur through acidic residues exposed along the outer surface in proximity to the iron entry pore. This narrow pore permits translocation of ions toward the ferroxidase centers via two discrete steps. Iron oxidation proceeds by transient formation of tri-iron ferroxidase centers. Iron storage by biomineralization inside the ferritin shell occurs at two iron nucleation centers. Here, a single iron atom provides a structural seed for iron-oxide cluster formation. The clusters with up to five iron atoms adopt a geometry that is different from natural biominerals like magnetite but resembles iron clusters so far known only from bioinorganic model compounds.