Life without oxygen is challenging, complex and how it all began some four billion years ago. A major constraint to heterotrophic life without oxygen is the disposal of electrons from the food they consume. Somewhere in Earth’s history bacteria invented a respiratory chain that could be linked to extracellular electron acceptors. These unique conduits facilitated disposal of electrons onto a range of redox active metal-containing minerals such as iron and manganese oxides through a process termed extracellular electron transfer (EET). EET is best understood in two gram-negative model bacterial systems, Shewanella oneidensis and Geobacter sulfurreducens. Many organisms capable of EET are also electroactive – meaning they can interface and form biofilms on poised electrode surfaces. We developed culture conditions and strain backgrounds where G. sulfurreducens is metabolically dependent on the anaerobic waste product of S. oneidensis. The quality or strength of electron dictates important dynamics of this system. Here we compare two co-culture systems, one based on conversion of glycerol to acetate, a capability engineered in S. oneidensis and another based on conversion of lactate to acetate. The metabolic rate of S. oneidensis is dramatically enhanced by the presence of G. sulfurreducens. We have evidence that several parallel mechanisms are at play, involving hydrogen, formate, electron shuttling and direct electron transfer. Understanding the parameters governing carbon and electron flow in anaerobic electroactive systems will enable both a fundamental understanding of how these microbial communities operate and provide insight into how to engineer them for a range of applications.