Conductive matrix architecture of sulfate-reducing bacteria boosts coculture electrical output

Abstract

Biogenic iron sulfide nanoparticles (FeS NPs) synthesized by sulfate-reducing bacteria (SRB) are prevalent in anoxic environments. The role these electrically conductive FeS NPs play in microbial interactions, however, remains undefined. We showed interactions between current producing microbes where Desulfovibrio vulgaris Hildenborough, a SRB, utilized FeS NPs to form long-range electron pathways in collaboration with Shewanella oneidensis MR-1, an iron-reducing bacteria. Single-potential amperometry showed synergetic current production associated with biogenic metallic FeS NPs with coculture of D. vulgaris and S. oneidensis compared to pure cultures. The synergetic current production in the coculture was diminished in the absence of biogenic FeS or with a mutant strain of S. oneidensis lacking genes encoding the electron transport pathway of the MtrCAB protein complex. Fluorescent in situ hybridization revealed the formation of cell-NP agglomerations that were twice as thick in cocultures as those from pure cultures, and the cell number of D. vulgaris was enhanced in the presence of S. oneidensis. Cell-NP agglomerations over 15 µm gap source–drain electrodes showed long-range current conduction in the coculture bioagglomerates specifically in the presence of metallic FeS. Additionally, nanoscale secondary ion mass spectroscopy revealed ¹⁵N and ¹³C assimilation, indicating sustained microbial metabolic activity in the cell-NP agglomerations. These data suggest that long-range electric conduction via biogenic FeS NPs enables SRB to cooperate with metabolically compatible partners, potentially activating the anaerobic SRB respiration that drives the global carbon and biogeochemical sulfur cycles.