Light-driven bioelectrical signaling in algal biofilms mediated by extracellular electron transfer networks

Open-circuit potentiometric measurements have recently emerged as non-invasive approach for monitoring bioelectrical signaling within microbial biofilms, preserving their structural and metabolic integrity. Although extracellular electron transfer (EET) networks in heterotrophic microbial communities are documented in the literature, their role in photosynthetic systems remains poorly understood. To determine whether photosynthetic microbial communities employ similar EET mechanisms and whether their electrical signaling can be described using resistance–capacitance (RC) circuit model validated for heterotrophic biofilms, a controlled aquatic experimental chamber containing sediment and aerobic zones was constructed, equipped with multiple microbial potentiometric sensors (MPS), inoculated with lake water and exposed to natural sunlight to promote eukaryote/prokaryote growth and biofilm formation. Open-circuit potential signals were monitored under varying light conditions and following deliberate disruption of algal biofilms on sensor surfaces. Two distinct signal types were observed. The observations suggest that α-signals are associated with mature algal mats, while β-signals are possibly generated by a single or possible shallow (oxygenated) stratum of photosynthetic biofilm. Both signals exhibited strong agreement with a modified RC circuit model using composite logistic functions (R 2 >0.995), suggesting that photosynthetic and heterotrophic microorganisms utilize a common EET network embedded within biofilms to transfer and temporarily store metabolic charge. A conceptual stratified-biofilm model for the algal mat is proposed in which photosynthetic organisms in upper layers serve as electron acceptor strata while deeper anaerobic microorganisms supply electrons through the shared EET network. These findings highlight a universal electrical framework for microbial charge transfer and suggest that biofilm-associated EET networks function as integrated charge transport systems supporting metabolic cooperation within microbial communities.