Flavin-based extracellular electron transfer under oxic conditions by Gram-positive Microbacterium deferre sp. nov. A1-JK in redox-graded environments

Abstract

Microbacterium deferre sp. nov. A1-JK is a metabolically versatile Gram-positive bacterium isolated from the oxic-anoxic interface of freshwater sediment, inhabited by cable bacteria. M. deferre A1-JK could simultaneously reduce oxygen and Fe(III), challenging the traditional view of microbial Fe(III)-reduction as a strictly anaerobic process. Electrochemical studies revealed extracellular electron transfer (EET) metabolism facilitated by soluble flavin shuttles, identified via HPLC. Genomic analyses uncovered EET pathways involving cytochrome FccA and flavin reductase FmnA. Its metabolic versatility also allowed for weak electroactivity in alkaline (pH 9-10) and saline conditions (0-4% NaCl). The ability to reduce Fe(III), in the presence of atmospheric oxygen highlights its adaptability to dynamic sediment environments with fluctuating oxygen and Fe(III) gradients. These findings underscore the metabolic versatility of M. deferre A1-JK at oxic-anoxic interfaces, providing insights into the coexistence of aerobic and anaerobic processes in a single cell. ImportanceMicrobacterium deferre A1-JK is a newly discovered gram-positive bacterium that employs flavin-mediated extracellular electron transfer to respire minerals and electrodes. Associated with cable bacteria in freshwater sediments, M. deferre A1-JK was able to simultaneously reduce oxygen and Fe(III). This makes it highly adaptable to changing environments, such as those found in (cable-bacteria-containing) sediments with fluctuating oxygen and Fe concentrations. The metabolic versatility of M. deferre A1-JK offers opportunities to fundamentally revise our understanding of microbial metabolism and nutrient cycling models that strictly separate aerobic and anaerobic metabolisms.