Microbial community mediates hydroxyl radical production in soil slurries by iron redox transformation

The generation of reactive oxygen species (ROS) mediated by minerals and/or microorganisms plays a vital but underappreciated role in affecting carbon and nutrient cycles at soil-water interfaces. It is currently unknown which interactions between microbial communities and iron (Fe) minerals produce hydroxyl radical (HO•), which is the strongest oxidant among ROS. Using a series of well-controlled anoxic incubations of soil slurries, we demonstrated that interactions between microbial communities and Fe minerals synergistically drove HO• production (up to ∼100 nM after 21-day incubation). Microorganisms drove HO• generation in anoxic environments predominantly by modulating iron redox transformation that was more prominent than direct production of ROS by microorganisms. Among the microbial communities, Geobacter, Paucimonas, Rhodocyclaceae_K82, and Desulfotomaculum were the key genera strongly affecting HO• production. In manured soils, the former two species had higher abundances and were crucial for HO• production. In contrast, the latter two species were mainly abundant and important in soils with mineral fertilizers. Our study suggests that abundant highly reactive oxidant HO• can be generated in anoxic environments and the microbial community-mediated redox transformations of iron (oxyhydr)oxides may be responsible for the HO• production. These findings shed light on the microbial generation of HO• in fluctuating redox environments and on consequences for global C and nutrient cycling.