Magnetite nanoparticles are metastable biogeobatteries in consecutive redox cycles driven by microbial Fe oxidation and reduction

Abstract

Iron (Fe) minerals play a crucial role in biogeochemical cycles due to their ubiquity in nature, high adsorption capacity and redox activity towards many other elements. Mixed-valent Fe minerals are unique since they contain Fe(II) and Fe(III). For example, magnetite (Fe(II)Fe(III)2O4) nanoparticles (MNPs) can affect the availability and mobility of nutrients and contaminants. This is due to the high surface area to volume ratio and the presence of Fe(II) and Fe(III), allowing redox transformation of (in‑)organic contaminants. Recent studies have shown that magnetite can serve as an electron source and sink for Fe(II)-oxidizing and Fe(III)-reducing microorganisms, storing and releasing electrons; thus, it functions as a biogeobattery. However, the ability of MNPs to act as biogeobatteries over consecutive redox cycles and the consequences for mineral integrity and identity remain unknown. Here, we show MNPs working as biogeobatteries in two consecutive redox cycles over 41 days. MNPs were first oxidized by the autotrophic nitrate-reducing Fe(II)-oxidizing culture KS and subsequently reduced by the Fe(III)-reducing Geobacter sulfurreducens. In addition to reduced magnetite, we identified the Fe(II) mineral vivianite after reductions, suggesting partial reductive dissolution of MNPs and re-crystallization of Fe2+ with phosphate from the growth medium. Measurements of the Fe(II)/Fe(III) ratio revealed microbial oxidation and reduction for both the first redox cycle (oxidation: 0.29±0.014, reduction: 0.75±0.023) and the second redox cycle (oxidation: 0.30±0.015, reduction: 1.64±0.10). Relative changes in magnetic susceptibility (∆κ in %) revealed greater changes for the second oxidation (–8.7±1.99%) than the first (–3.9±0.19%) but more minor changes for the second reduction (+14.29±0.39%) compared to the first (+25.42±1.31%). Our results suggest that MNPs served as biogeobatteries but became less stable over time, which has significant consequences for associated contaminants, nutrients and bioavailability for Fe-metabolizing microorganisms.