Microbial electrosynthesis is a renewable energy and chemical production platform that relies on microbial cells to capture electrons from a cathode and fix carbon. Yet despite the promise of this technology, the metabolic capacity of the microbes that inhabit the electrode surface and catalyze electron transfer in these systems remains largely unknown. We assembled thirteen draft genomes from a microbial electrosynthesis system producing primarily acetate from carbon dioxide, and their transcriptional activity was mapped to genomes from cells on the electrode surface and in the supernatant. This allowed us to create a metabolic model of the predominant community members belonging to Acetobacterium, Sulfurospirillum, and Desulfovibrio. According to the model, the Acetobacterium was the primary carbon fixer, and a keystone member of the community. Transcripts of soluble hydrogenases and ferredoxins from Acetobacterium and hydrogenases, formate dehydrogenase, and cytochromes of Desulfovibrio were found in high abundance near the electrode surface. Cytochrome c oxidases of facultative members of the community were highly expressed in the supernatant despite completely sealed reactors and constant flushing with anaerobic gases. These molecular discoveries and metabolic modeling now serve as a foundation for future examination and development of electrosynthetic microbial communities.A microbial electrosynthesis system (MES) is a bioelectrochemical device that employs microbes to generate, or synthesize, valuable products from CO 2 and electrons from the cathode 1 . This technology has potential for the renewable generation of biofuels and commodity chemicals, therefore understanding which microbes and which metabolic pathways are involved on biocathodes is critical to improving the performance of MESs. Furthermore, this work has broader environmental implications including understanding ecological aspects of one carbon metabolism and extracellular electron transfer relevant to global biogeochemical cycling.Advances in microbial electrosynthesis and related biocathode-driven processes have primarily focused on the production of three compounds: hydrogen 2 , methane 3 , and acetate 4 . However, microbial electrosynthesis can be used to generate value-added multi-carbon compounds such as alcohols and various short-chain fatty acids 5 . To manipulate (and optimize) these systems it is valuable to understand the metabolic pathways and extracellular electron transfer (EET) enzymes or molecules involved in cathode oxidation, and we must determine how these cathodic electron transport components are coupled to energy conservation by the microbial cell. While an increasingly robust body of literature has been established relating to microbial communities metabolizing with an anodic electron acceptor 6-8 , much is still unclear about the diverse metabolic capabilities of microorganisms and communities growing on a cathode 9 . Recently, a multi-omics evaluation of a mixed-species, carbon