Bidirectional extracellular electron transfer and electroautotrophic metabolism in Fundidesulfovibrio terrae

Extracellular electron transfer (EET) is a pivotal process in biogeochemical and bioelectrochemical systems, where its bidirectional form governs microbial energy exchange in complex environments. Sulfate-reducing bacteria (SRB) exhibit notable metabolic flexibility via bidirectional EET, yet this trait has been verified in only a few species. Herein, we report the bidirectional EET capability and electroautotrophic carbon fixation potential of a newly isolated SRB, Fundidesulfovibrio terrae SG127. This strain exhibited remarkable extracellular Fe(III) reduction activity, with a maximum reduction ratio of 68.3% in 7 d. Electrochemical measurements confirmed that the strain is capable of bidirectional EET, as evidenced by the generation of a maximum anodic and cathodic current density of 27.50 and 28.75 μA/cm2 through donating electrons to and accepting them from the electrode, respectively. A combination of UV-vis spectroscopy, inhibition studies, and genomic analyses confirmed the key role for c-type cytochromes in mediating bidirectional EET in F. terrae. Under autotrophic conditions, F. terrae efficiently converts CO2 into acetate as the main product by utilizing electrons from the electrode via a controlled potential in a microbial electrosynthesis system, attaining an acetate concentration of up to 11.05 mM. These findings provide a novel microbial resource and theoretical foundation for understanding the role of microorganisms in the carbon cycle, and for developing microbial electrochemical strategies to achieve carbon neutrality.