Nature's first electrical tool: microbial biofilms using electron transfer networks to perform aerobic respiration in an anaerobic environment

Heterotrophic biofilms in an anaerobic chamber exhibit characteristics consistent with extracellular electron transfer (EET) networks capable of storing electrons and transporting them to atmospheric oxygen as the ultimate electron acceptor. Considering this charge storage phenomenon of biofilms, it was hypothesized that EET networks in biofilms would behave like resistor-capacitor (RC) circuits. To test this hypothesis, an experimental system equipped with 48 microbial potentiometric sensor (MPS) electrodes and four reduction/oxidation probes (ORP) was briefly disturbed by introducing a pulse of electron donor compound (acetate), and the generated potentials were monitored over several months to validate a theoretical model that was developed and described the behaviors of RC circuits. The data suggested existence of two electrically isolated systems (biofilm and bulk solution) where the biofilm matrix served as a long-range electrical conduit employed by the biofilm microorganisms in a two-step process: (1) temporary storage of metabolic charge in the temporary electron acceptors (TEAs) within the EET network (assimilation phase) poised at higher potentials than the soluble electron acceptors, and (2) the subsequent transfer of this temporarily stored charge through the electrical gradients of the EET mechanisms (dissipation phase) to ultimate electron acceptor (oxygen) located at a distance. The developed RC model based on a generalized logistic function (Richard's function) described this biofilm behavior with high precision. In brief, the entire biofilm system represents an extracellular “electrical tool” for performing an aerobic respiration in an anaerobic environment. The presented results therefore strongly imply that the observed RC arrangement is compatible with generation of a biological field as nature's first tool for maximizing energy utilization.