Probing the biotransformation of hematite nanoparticles and magnetite formation mediated by Shewanella oneidensis MR-1 at the molecular scale

摘要

Although the existence of Fe(III) (hydr)oxide nanoparticles (NPs) in natural environments has been recently recognized, their migration and transformation, which are substantially affected by the microbial reduction process, remain unclear. In this study, hematite bioreduction and magnetite formation induced by Shewanella oneidensis MR-1, a typical metal-reducing bacterial strain, were investigated using an integrated approach that combined experiments and computational simulations at the molecular scale. High-resolution transmission electron microscopy coupled with selected area electron diffraction (SAED), Raman spectroscopy and magnetic property analyses confirmed the biogenic magnetite formation. The electron paramagnetic resonance (EPR) spectra show a decay of the EPR intensity with incubation time, implying that the biotransformation of hematite to magnetite led to concurrent changes in their contents and local structures. X-ray absorption fine spectroscopy (XAFS) identified a time-resolved structural evolution of Fe(II)/Fe(III) coordination. The octahedral configuration upon Fe(II) production was subsequently validated by DFT calculations. Microbial reductive dissolution provided various intermediate states and new chemical environments regarding Fe(II)/Fe(III) complexes, such as monodentate and bidentate coordination patterns. Bioreduction caused the breakage of ironoxygen bonds in hematite and the concomitant formation of Fe complexing microstructures for biogenic magnetite production. All these findings reveal the underlying mechanisms for the biotransformation of Fe minerals at the molecular scale and may allow us to better understand the speciation, immobilization and bioavailability of hematite NPs in natural systems.