Multi-Omics Reveal Extracellular Electron Transfer Mechanism Under Deep-Sea High Salinity

Microorganism-mineral interaction is crucial for understanding the degradation of organic matter involved in the electron exchange in marine sediments. Widespread metal-reducing bacteria Shewanella spp. have a unique ability of extracellular electron transfer (EET); however, their EET activity and underlying mechanisms under high-salinity stress in the deep sea remain poorly explored. Here, we studied the EET process and the underlying metabolic mechanism based on a deep-sea bacterium Shewanella piezotolerans WP3. S. piezotolerans WP3 has comparable electroactivity to the model strain S. oneidensis MR-1, achieving a maximum current density of 9.7 ± 0.7 μA/cm² at 0.6 V vs. Ag/AgCl. Multiheme-cytochrome OmcA-MtrCAB complex contributed to the direct EET, with mtrB, mtrA and omcA-1 upregulated and the redundant omcA genes (i.e., omcA-4, omcA-3) exhibiting low expression. Riboflavin, synthesised from guanosine triphosphate under high-salinity conditions, was secreted to facilitate EET. Enhanced glycolysis and TCA cycle activities under high anode potential (0.6 V) were confirmed by the downregulation of intermediate metabolites (e.g., phosphoenolpyruvate) and the upregulation of corresponding genes (e.g., pyk), supporting the high energy yield for the EET process. Our findings provide new insights into the EET mechanisms of marine Shewanella, paving the way for the development of bioelectronic sensors and biotechnology applications in high-salinity wastewater.