Conjugated Polymer‐Microbe Interactions Trigger Regulatory Reprogramming for Enhanced Bioelectrocatalysis

Abstract

ABSTRACT 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.