Phenolics are among the most abundant redox-active organics in nature, but the intractability of phenolic materials (e.g., melanin) has precluded study of their biological activities and functions. Previous studies demonstrated that a model abiotic catecholic matrix can rapidly exchange electrons with biological oxidants and reductants without the need for enzymes. Here, a novel electrochemically based reverse engineering approach was employed to probe redox interactions between this model matrix and a population of bacteria. Specifically, this method employs redox-active natural products (e.g., pyocyanin) to shuttle electrons between the bacteria and the abiotic matrix, and imposed oscillating potential inputs to engage redox-cycling mechanisms that switch the matrix's redox state. The oscillating output currents were observed to be amplified, gated, and partially rectified, while the overall magnitude and direction of electron flow across the matrix depended on the biological and environmental context. These response characteristics support hypotheses that natural phenolic materials may be integral to extracellular electron transport for processes that include anaerobic respiration, redox signaling, and redox-effector action.