Redox gradients in marine sediments serve as a fundamental energetic driver for microbial electron transfer and elemental biogeochemical cycling. However, their ecological impacts are tightly coupled to substrate availability, mass transport processes, and sediment heterogeneity, posing substantial challenges for disentangling their independent effects under in situ conditions. In this study, sediment samples collected from three deep-sea stations in the Western Pacific Ocean were used as microbial inocula. Controlled artificial potential gradients were established via the application of external voltages of 0.3 V, 0.5 V, and 0.7 V to simulate redox differentiation in natural marine sediments. A multi-technical approach integrating real-time current monitoring, 16S rRNA gene amplicon sequencing and untargeted metabolomics was employed to elucidate how artificial potential gradients modulate sedimentary electron transfer dynamics, microbial community assembly, and metabolic functional profiles. Nearly no detectable current was generated under the 0.3 V treatment, whereas sustained current production was observed at 0.5 V and 0.7 V, demonstrating a clear potential-dependent activation of sedimentary electron transfer processes. The redox gradients markedly reshaped the composition of bacterial communities and selectively enriched putative electroactive microbial taxa, including Arcobacter, Marinobacter, Shewanella, and Geoalkalibacter. In contrast, archaeal communities exhibited relatively high structural resistance to short-term electrochemical perturbations. The most pronounced metabolic shifts occurred during the transition from low to intermediate potential differences, primarily involving pathways associated with aromatic compound degradation, cofactor metabolism, amino acid metabolism, and nucleotide metabolism. Collectively, the sediment microbiome exhibited a staged state transition in response to externally imposed redox gradients in this experimental system. Specifically, increasing the applied voltage from 0.3 V to 0.5 V drove a pivotal community shift from a mode dominated by local substrate transformation to sustained electrode-coupled electron transfer. These findings demonstrate that sediment redox gradients function not only as environmental filters for microorganisms with specialized electron-transfer capabilities, but also as key regulators of electrode-associated spatial niche partitioning and metabolic resource allocation. Such gradient-dependent effects further modulate electron partitioning within sediment matrices and its coupling to elemental biogeochemical cycles. This study establishes a robust experimental framework for understanding the organizational mechanisms of sedimentary electron flow and its underlying biogeochemical implications in the natural sedimentary “biogeobattery” system.
 

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