Revealing the roles of chemical communication in restoring the formation and electroactivity of electrogenic biofilm under electrical signaling disruption

Electrogenic biofilms in microbial electrochemical systems have played significant roles in simultaneous wastewater treatment and energy recovery owing to their unique extracellular electron transfer. Their formation has been shown to be regulated by electrical and chemical communication, but the interaction between these signal communication pathways has not been studied. This research investigated the coordination between intracellular c-di-GMP signaling and reinforced quorum sensing with or without exogenous HSL (a common quorum sensing molecule), on the formation of mixed-cultured electrogenic biofilm under electrical signaling disruption by tetraethylammonium (TEA, a broad-range potassium channel blocker). Intracellular c-di-GMP was spontaneously reinforced in response to TEA stress, and metagenomic analysis revealed that the dominant DGC (the genes for producing c-di-GMP) induced the eventual biofilm formation by mediating exopolysaccharide synthesis. Meanwhile, reinforced quorum sensing by exogenous HSL could also benefit the biofilm restoration, however, it alleviated the TEA-induced communication stress, resulting in the weakening of c-di-GMP dominance. Interestingly, suppressing electrical communication with or without HSL addition both induced selective enrichment of Geobacter of 85.5% or 30.1% respectively. Functional contribution analysis revealed the significant roles of Geobacter and Thauera in c-di-GMP signaling, especially Thauera in resistance to TEA stress. This study proposed a potential strategy for electrogenic biofilm regulation from the perspectives of cell-to-cell communication.