Microbial electrosynthesis is a metabolic process in which extracellular electrons are utilized as the primary energy source for carbon fixation. While microbial electrosynthesis has been proposed as a novel concept for ecological primary production, our understanding of how such microorganisms are distributed in natural environments remains limited. In this study, we constructed a laboratory-scale electrochemical cultivation system that simulates electric discharge conditions in deep-sea hydrothermal fields. Microscopic counts revealed increased cell numbers in the electrochemical culture, and 16S rRNA gene analysis revealed a significant enrichment of a novel Thiomicrorhabdus species. Quantitative PCR confirmed proliferation and enrichment of a metagenome-assembled genome (MAG), named the SREC-4. Electrochemical cultivation with 13C-labeled CO₂ as a substrate indicated significant 13C incorporation specifically in Thiomicrorhabdus cells including MAG SREC-4. The genome of MAG SREC-4 revealed the possession of the putative extracellular electron uptake pathway in addition to the autotrophic sulfur-oxidizing aerobic respiration pathways typically found in Thiomicrorhabdus members. The putative extracellular electron uptake pathway was found in a phylogenetic clade in Thiomicrorhabdus mainly formed by strains derived from hydrothermal fields. These results provide the direct experimental evidence from enrichment cultures derived from hydrothermal fields that an organism inhabiting deep-sea hydrothermal fields can grow electrosynthetically, and suggest that this ability is shared by other Thiomicrorhabdus species, specifically those found in similar environments. This finding suggests electrosynthetic growth may be widely distributed in Thiomicrorhabdus populations dwelling in deep-sea hydrothermal fields, the largest natural electrogenic environment on Earth.
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