Complete uranium bioreduction in 48 hours: Synergistic electron transfer in a synthetic microbial consortium

Uranium contamination from mining and natural sources poses a major environmental and health risk, as soluble uranium U(VI) readily migrates through groundwater systems. Microbial reduction to insoluble U(IV) via dissimilatory metal-reducing bacteria offers a sustainable remediation method, relying on extracellular electron transfer (EET) to shuttle electrons to extracellular acceptors. <i>Shewanella oneidensis</i> MR-1 (<i>S</i>.MR-1) serves as a model organism for this process, but its EET efficiency is hindered by limited endogenous redox mediators and biofilm conductivity. Despite advances in genetic engineering, the potential of synthetic microbial communities to enhance EET through interspecies interactions remains underexplored. Here we show a synthetic consortium comprising <i>S</i>.MR-1 and a non-U-reducing isolate, <i>Pseudomonas aeruginosa</i> LXZ1 (<i>P</i>.LXZ1), that fully reduces U(VI) within 48 h, compared to only 60 % reduction by <i>S</i>.MR-1 alone. This enhancement stems from <i>P</i>.LXZ1-secreted pyocyanin, which binds selectively to <i>S</i>.MR-1's outer-membrane cytochrome OmcA, shifting its redox potential to facilitate directional electron flow along a thermodynamic gradient. Concurrently, conductive extracellular DNA released by <i>P</i>. LXZ1 promotes electron transport and aggregate formation, as evidenced by electrochemical assays, transcriptomics, and molecular dynamics simulations. These synergistic mechanisms alleviate proton-transfer limitations and upregulate metabolic pathways, boosting overall EET rates. By harnessing natural microbial cooperation, this approach provides insights into community-driven metal reduction and paves the way for efficient, scalable bioremediation strategies in contaminated sites.