Oxic microbial ferrihydrite reduction rates of Shewanella oneidensis and the potential for Fe mobilization in oxic sediments

Abstract

Microbially mediated reduction of ferrihydrite (Fe(III) oxyhydroxide) plays a crucial role in Fe cycling, and hence nutrient and contaminant cycling, in subsurface environments. This process is typically considered a strictly anaerobic process confined to anoxic microsites within oxic subsurface environments. However, recent findings suggest that microbes can also mediate ferrihydrite reduction under oxic conditions. Here, we quantified cell-specific rates of ferrihydrite reduction by the model organism Shewanella oneidensis MR-1 under oxic and anoxic conditions. We used these rates to assess the relative contribution of oxic and anoxic pore spaces to Fe(II) mobilization in a previously published laboratory analog of oxic aquifer sediments. Oxic reduction proceeded persistently, albeit at a per cell rate 100 times more slowly than anoxic reduction, yet still generated appreciable Fe(II). Modeling suggests that when anoxic microsites are absent or occupy a minor fraction of the pore space, oxic Fe(III) reduction can account for a significant share of total Fe(II) release. Such conditions are common in shallow aquifers, well-drained soils, and capillary fringes. We conclude that oxic Fe(III) reduction is a persistent background process that has been underestimated in current biogeochemical frameworks.

Supplementary Information: The online version contains supplementary material available at 10.1038/s41598-025-16963-w.

Keywords: Shewanella oneidensis; Anoxic microsites; Ferrihydrite; Microbial iron reduction; Oxic sediments; Oxygen.

Fig. 1

(a) Representation of a porous oxic subsurface environment. (b) Zoom in of the pore space and solid grains with attached biofilms of variable thicknesses controlled by the solid matrix structure and pore water flow. Depending on the thickness of the biofilm, which mostly controls the microscale balance between O₂ transport and the intensity of aerobic respiration, the biofilm, whose perimeter is indicated as a green dashed line in panels c and d, may remain permanently oxygenated (c) or host the formation of an anoxic microsite (d).

Fig. 2

(a) Evolution of Fe(II) concentrations in oxic and anoxic S. oneidensis incubations and the corresponding killed controls every 24 h for 144 h. A vertical bar indicates the standard deviation computed over triplicates. Results for negative controls are reported in SI (Section S2). Dashed lines indicate the linear interpolation of Fe(II) concentrations. (b) Evolution of O₂ concentrations measured every 10 min by an optical spot sensor in oxic S. oneidensis incubations, reported as the average over the 3 replicates. The shaded area indicates the standard deviation around the average. For comparison, O₂ concentrations measured in one replicate of the killed control are reported (black dots). Time t = 0 h corresponds to ferrihydrite and FZ addition to S. oneidensis cultures.

Fig. 3

(a) Cell concentrations (± standard deviation) of S. oneidensis computed for the initial inoculum and after 48 h of incubation under oxic and anoxic conditions. (b) Ferrihydrite, Fe(III), reduction rate per cell (± standard deviation) under oxic and anoxic conditions.

Fig. 4

(a) Pore space volume occupied by oxic biomass (V_O) and anoxic microsites (V_A) as a function of time computed from data in. (b) Temporal trend of the relative contribution of oxic biomass (c_O) and anoxic microsites (c_A) to the overall Fe(II) mobilization rate during the experiment (Eq. (2), Section “Probabilistic assessment of Fe(II) mobilization in oxic sediments”). (c) Cumulative relative contribution of Fe(II) mobilized by anoxic microsites (C_A) and by oxic biomass (C_O) during the entire duration of the experiment (45 h), i.e., c_o and c_a integrated over time for 45 h (Eq. (3), Section “Probabilistic assessment of Fe(II) mobilization in oxic sediments”).

Fig. 5

Sketches of S. oneidensis incubation setups under oxic conditions(a) and anoxic conditions (b).