Convergent Biogenic Magnetite Formation from Diverse Iron (Oxyhydr)oxide Precursors Drives Cr(VI) Reduction via an Environmental Battery Mechanism

Iron (oxyhydr)oxides mediate electron flux across coupled biogeochemical cycles in anoxic environments, yet whether their biogenic transformation feeds back to reshape interfacial electron transfer efficiency remains unresolved. Here, five structurally distinct iron (oxyhydr)oxide precursors (ferrihydrite, goethite, magnetite, wüstite, and hematite) were exposed to anaerobic sulfur-oxidizing bioreactors under Cr(VI) stress, and their transformation trajectories were tracked using synchrotron EXAFS spectroscopy, electrochemical impedance spectroscopy, DFT calculations, and metagenomic profiling. Mineral bioavailability decreased in the order ferrihydrite > goethite > magnetite > wüstite > hematite, a hierarchy governed by lattice iron-leaching energetics quantified via DFT (Efev from -8.96 eV for ferrihydrite to 5.76 eV for hematite). Despite this wide disparity in precursor lability, all biotransformation trajectories converged on magnetite as the thermodynamically stable end point. In the ferrihydrite system, biogenic magnetite reached 60% of the final solid phase and operated as an in situ "environmental battery" (storing and releasing electrons through reversible Fe(II)/Fe(III) lattice cycling), lowering interfacial charge transfer resistance and producing a 4.77-fold higher pseudo-first-order Cr(VI) reduction rate constant than the mineral-free biotic control (C-S). Metagenomic analysis revealed mineral-specific restructuring of the microbial community toward a tightly coupled sulfur-iron redox network. These results reframe precursor mineralogy from a determinant of intrinsic reactivity to a kinetic regulator of biogenic electron-buffer formation, providing a mechanistic basis for mineral-informed bioremediation design.