Conjugated Polymer-Microbe Interactions Trigger Regulatory Reprogramming for Enhanced Bioelectrocatalysis

Abiotic redox-active materials are increasingly used to interface with electroactive microorganisms, yet their influence on cellular regulation remains poorly understood. Here, Shewanella oneidensis MR-1 was coupled with the electron-transporting conjugated polymer poly(benzodifurandione) (PBFDO) to examine how material interfaces reshape inward extracellular electron transfer (EET). PBFDO-coated carbon electrodes enhanced electron uptake and fumarate reduction, producing over two orders of magnitude higher current density and up to a twelvefold increase in succinate production than polymer-free controls. Integrated electrochemical, transcriptomic, metabolomic, and protein analyses reveal coordinated physiological remodeling associated with the polymer-supported interface rather than passive conductivity alone. PBFDO exposure is associated with transcriptional enrichment of genes linked to the Mtr-CymA electron-transfer conduit, energy metabolism, and biofilm formation. Metabolomics revealed altered intracellular redox and metabolite profiles consistent with enhanced fumarate respiration, alongside elevated NADH/NAD⁺ and ATP/ADP ratios indicative of altered cellular redox and energetic states. Beyond transcriptional regulation, polymer-responsive small RNAs (sRNAs) revealed a post-transcriptional regulatory layer linked to the biohybrid interface. Delivery of individual sRNAs into control cells partially recapitulated the polymer-induced phenotype, increasing current output up to threefold while altering intracellular redox balance. These findings establish sRNA-mediated regulation as a previously unrecognized mechanism linking biohybrid interfaces to enhanced microbial electrosynthesis.