Investigating Nanoscale Electron Transfer Processes at the Cell-Mineral Interface in Cobalt-Doped Ferrihydrite Using Geobacter sulfurreducens: A Multi-Technique Approach

Abstract

Cobalt is an essential element for life and plays a crucial role in supporting the drive to clean energy, due to its importance in rechargeable batteries. Co is often associated with Fe in the environment, but the fate of Co in Fe-rich biogeochemically-active environments is poorly understood. To address this, synchrotron-based scanning X-ray microscopy (SXM) was used investigate the behaviour of cobalt at the nanoscale in Co-Fe(III)-oxyhydroxides undergoing microbial reduction. SXM can assess spatial changes in metal speciation and organic compounds helping to elucidate the electron transfer processes occurring at the cell-mineral interface and inform on the fate of cobalt in redox horizons. G. sulfurreducens was used to reduce synthetic Co-ferrihydrite as an analogue of natural cobalt-iron-oxides. Magnetite [Fe(II)/Fe(III)3O4] production was confirmed by powder X-ray diffraction (XRD), SXM and X-ray magnetic circular dichroism (XMCD) data, where best fits of the latter suggested Co-bearing magnetite. Macro-scale XAS techniques suggested Co(III) reduction occurred and complementary SXM at the nanoscale, coupled with imaging, found localised biogenic Co(III) reduction at the cell-mineral interface via direct contact with outer membrane cytochromes. No discernible localised changes in Fe speciation were detected in the reordered cobalt-iron-oxides that were formed and at the end point of the experiment only 11% Co and 1.5% Fe had been solubilised. The solid phase retention, alongside the highly localised and preferential cobalt bioreduction observed at the nanoscale is consistent with retention of Co in redox zones. This work improves our fundamental molecular-scale understanding of the fate of Co in complex environmental systems and supports the development of biogenic Co-doped magnetite for industrial applications from drug delivery systems to magnetic recording media.

Diversity of Iron Oxides: Mechanisms of Formation, Physical Properties and Applications

“…Both plants and microbes offer various ways to synthesize magnetite and maghemite NPs for potential dye degradation from industrial effluents from a variety of routes due to their vast genetic diversity and presence of various enzymes, respectively [420]. Co-substituted magnetite NPs were produced during the enzymatic reduction of a synthetic co-ferrihydrite using Geobacter sulfurreducens as an analogue to bioreduction processes in the natural environment to understand the natural biogeochemical cycling of cobalt in Fe-rich environments undergoing microbially mediated redox transformations [421]. Natural biogenic iron oxide extracted from banded iron formations showed high removal potential with the maximum sorption efficiency of 88.65% at a 30 g/L adsorbent dose [422].…”

The value of synchrotron radiation X‐ray techniques to explore microscale chemistry for ecology and evolution research

“…Furthermore, SXM and STXM are also often powered by SR and have the unique ability to identify and mark key protein and carbohydrate structures within a sample. These techniques can enable the user to examine the speciation chemistry of both an inorganic phase (e.g., mineral) and an organic phase (e.g., bacterial specimen) simultaneously (Buchanan et al, 2022; Schmid et al, 2016). As with XPS, STXM is particularly useful for visualizing biofilm or microbial species' dynamics but has also been used for characterizing the chemistry of bioaerosols, working at a high spatial resolution again (<40 nm; China et al, 2020).…”