Electricity generation and shifts in methanogenesis mediated by an oil-field-derived electroactive bacterium in legacy tar pit sediments

Microbial fuel cells (MFCs) have been proposed as a sustainable technology for energy recovery from organic matter; however, the ecological roles of electroactive bacteria (EAB) in oil field environments and their relationships with methanogenic processes remain incompletely understood. In this study, we isolated a novel Fe(III)-reducing bacterium, designated as the strain NKC854, from a legacy tar pit environment and examined its potential contribution to electricity generation in laboratory-scale single-chamber sediment MFCs, field-relevant sediment systems in sediment MFCs, and electrochemical cultivation to determine the electroactivity of the strain. Power generation was observed in the oil field-installed MFC, with the maximum current density of 189 mA m−2. In laboratory sediment MFCs, the highest current density was also observed in 2-bromoethanesulfonate solution (2-BES)-amended systems (534 mA m⁻²) during the early operational phase, suggesting that changes in microbial activity can redirect electrons toward the anode. Carbon flux analysis indicated that electricity generation was associated with increased CO₂ production, whereas methane formation predominated when readily biodegradable substrates such as yeast extract were supplied. Yeast extract addition stimulated methane production more strongly than electricity generation, implying preferential utilization of readily biodegradable organic substrates by methanogenic pathways. Microbial community analysis revealed the selective enrichment of a novel Geobacter sp. on anodes of current-generating oil field-installed and laboratory sediment MFCs, while it remained undetectable in control and open-circuit systems. A Fe (III)-reducing strain was isolated from the tar pit sediment, and the 16S rRNA gene sequence of the isolated strain completely corresponded with the most dominant sequence on current-generated anodes of lab-scale and oil-field MFCs. The strain exhibited stable current generation under acetate-fed electrochemical conditions. This study provides insight into the ecophysiology of a novel electroactive microorganism activated in a crude oil-polluted site and the allocation of microbial electrons in hydrocarbon-impacted sediments, suggesting a competition between microbial activity related with methanogenesis and electricity interactions.