Microbial interspecies electron transfer via electric currents through conductive minerals

Abstract

In anaerobic biota, reducing equivalents (electrons) are transferred between different species of microbes [interspecies electron transfer (IET)], establishing the basis of cooperative behaviors and community functions. IET mechanisms described so far are based on diffusion of redox chemical species and/or direct contact in cell aggregates. Here, we show another possibility that IET also occurs via electric currents through natural conductive minerals. Our investigation revealed that electrically conductive magnetite nanoparticles facilitated IET from Geobacter sulfurreducens to Thiobacillus denitrificans, accomplishing acetate oxidation coupled to nitrate reduction. This two-species cooperative catabolism also occurred, albeit one order of magnitude slower, in the presence of Fe ions that worked as diffusive redox species. Semiconductive and insulating iron-oxide nanoparticles did not accelerate the cooperative catabolism. Our results suggest that microbes use conductive mineral particles as conduits of electrons, resulting in efficient IET and cooperative catabolism. Furthermore, such natural mineral conduits are considered to provide ecological advantages for users, because their investments in IET can be reduced. Given that conductive minerals are ubiquitously and abundantly present in nature, electric interactions between microbes and conductive minerals may contribute greatly to the coupling of biogeochemical reactions.

Fig. 1.

Electrochemical characteristics of G. sulfurreducens (blue lines) and T. denitrificans (black lines) on ITO electrodes. Anodic currents were measured using an electrode poised at +0.4 V vs. SHE after supplemented with 20 mM acetate (A), whereas cathodic currents were measured at −0.4 V vs. SHE with 30 mM nitrate (B). Linear sweep voltammograms (C) were measured at a scan rate of 1 mV s⁻¹ 30 h after initiating the incubation.

Fig. 2.

Changes in substrates and metabolites in single cultures of G. sulfurreducens (blue dashed lines), single cultures of T. denitrificans (black dashed lines), and their cocultures (red solid lines) in the absence (A) and presence (B–E) of different mineral species (indicated above the graphs) or in controls supplemented with Fe ion (F). Changes in concentrations of nitrate (diamonds), acetate (circles), and ammonium (triangles) are shown. Data points represent means of three independent cultures; error bars indicate SDs.

Fig. 3.

Cumulative curves showing amounts of electrons (mM equivalent) transferred from G. sulfurreducens to T. denitrificans. Data points represent means of three independent cultures; error bars indicate SDs.

Fig. 4.

SEM images for precipitates formed in cocultures of G. sulfurreducens and T. denitrificans 6 d after initiating the cultivation in the absence (A) and presence (B and C) of magnetite. Points at which EDX spectra were obtained are indicated in C (immediately left of the blue boxes), whereas EDX spectra are shown in D (a yellow area, spectrum 1 for the upper point in C; a red line, spectrum 2 for the lower point). (Scale bars: 1 μm.)