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

Abstract

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.

Keywords: Fenton reaction; Iron minerals; Microorganism-mineral interactions; Reactive oxygen species; Synergistic effect.