Background: Interspecies hydrogen transfer (IHT) and direct interspecies electron transfer (DIET) are two syntrophy models for methanogenesis. Their relative importance in methanogenic environments is still unclear. Our recent discovery of a novel species Candidatus Geobacter eutrophica with the genetic potential of IHT and DIET may serve as a model species to address this knowledge gap. Results: To experimentally demonstrate its DIET ability, we performed electrochemical enrichment of Ca. G. eutrophica-dominating communities under 0 and 0.4 V vs. Ag/AgCl based on the presumption that DIET and extracellular electron transfer (EET) share similar metabolic pathways. After three batches of enrichment, acetate accumulated in all reactors, while propionate was detected only in the electrochemical reactors. Four dominant fermentative bacteria were identified in the core population, and metatranscriptomics analysis suggested that they were responsible for the degradation of fructose and ethanol to propionate, propanol, acetate, and H2. Geobacter OTU650, which was phylogenetically close to Ca. G. eutrophica, was outcompeted in the control but remained abundant and active under electrochemical stimulation. The results thus confirmed Ca. G. eutrophica’s EET ability. The high-quality draft genome (completeness 99.4%, contamination 0.6%) further showed high phylogenomic similarity with Ca. G. eutrophica, and the genes encoding outer membrane cytochromes and enzymes for hydrogen metabolism were actively expressed. Redundancy analysis and a Bayesian network constructed with the core population predicted the importance of Ca. G. eutrophica-related OTU650 to methane production. The Bayesian network modeling approach was also applied to the genes encoding enzymes for alcohol metabolism, hydrogen metabolism, EET, and methanogenesis. Methane production could not be accurately predicted when the genes for IHT were in silico knocked out, inferring its more important role in methanogenesis.Conclusions: Ca. G. eutrophica is electroactive and simultaneously performs IHT and DIET. The results from the metatranscriptomic analysis have provided valuable information for enrichment and isolation of Ca. G. eutrophica. IHT is predicted to have a stronger impact on methane production than DIET in the electrochemical reactors. The genomics-enabled machine learning modeling approach can provide predictive insights into the importance of IHT and DIET.