Microbially mediated manganese (Mn) oxidation is a key process in the biogeochemical cycling of Mn. While Shewanella is widely recognized for its metal-reducing capabilities, recent studies have shown that certain terrestrial strains can also oxidize Mn2+ during aerobic respiration. Nevertheless, the Mn2+-oxidizing capacity of marine Shewanella strains, which are ubiquitous in oceanic settings, has remained largely unexplored, and the influence of environmental factors on this capacity has not been systematically evaluated. Here, we investigated the ability of the deep-sea bacterium S. piezotolerans WP3 to oxidize Mn2+ under aerobic conditions and examined the effects of temperature (4°C-20°C) and hydrostatic pressure (0.1-20 MPa). We found that S. piezotolerans WP3 efficiently oxidizes Mn2+ to Mn oxides, predominantly forming bixbyite-like minerals and amorphous mixed-valence nanoparticles. This oxidation process was not attributable to a Mn2+-specific enzyme but to bacterially generated reactive oxygen species (ROS), with superoxide (O2 •-) playing the primary role. Both temperature and hydrostatic pressure significantly affected the final extent of Mn2+ oxidation by altering the production of O2 •-. Transcriptomic analysis revealed that exposure to high hydrostatic pressure induced the upregulation of genes involved in antioxidative stress, which likely accounts for the enhanced ROS-mediated Mn2+ oxidation observed in cultures incubated at 20 MPa. Under alternating aerobic and anaerobic conditions, strain WP3 mediated successive Mn oxidation and reduction, ultimately forming rhodochrosite as a secondary mineral. These results suggest that S. piezotolerans WP3 has the potential to mediate Mn redox cycling in marine sediments, coupling ROS-dependent oxidation with anaerobic Mn reduction.
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