Electron Hopping Enables Rapid Electron Transfer between Quinone-/Hydroquinone-Containing Organic Molecules in Microbial Iron(III) Mineral Reduction

The mechanism of long-distance electron transfer via redox-active particulate natural organic matter (NOM) is still unclear, especially considering its aggregated nature and the resulting low diffusivity of its quinone- and hydroquinone-containing molecules. Here we conducted microbial iron(III) mineral reduction experiments in which anthraquinone-2,6-disulfonate (AQDS, a widely used analogue for quinone- and hydroquinone-containing molecules in NOM) was immobilized in agar to achieve a spatial separation between the iron-reducing bacteria and ferrihydrite mineral. Immobilizing AQDS in agar also limited its diffusion, which resembled electron-transfer behavior of quinone- and hydroquinone-containing molecules in particulate NOM. We found that, although the diffusion coefficient of the immobilized AQDS/AH₂QDS was 10 times lower in agar than in water, the iron(III) mineral reduction rate (1.60 ± 0.28 mmol L⁻1 Fe(II) d⁻¹) was still comparable in both media, indicating the existence of another mechanism that accelerated the electron transfer under low diffusive conditions. We found the correlation between the heterogeneous electron-transfer rate constant (10⁻³ cm s⁻¹) and the diffusion coefficient (10⁻⁷ cm² s⁻¹) fitting well with the "diffusion-electron hopping" model, suggesting that electron transfer via the immobilized AQDS/AH₂QDS couple was accomplished through a combination of diffusion and electron hopping. Electron hopping increased the diffusion concentration gradient up to 10⁶-fold, which largely promoted the overall electron-transfer rate during microbial iron(III) mineral reduction. Our results are helpful to explain the electron-transfer mechanisms in particulate NOM.