Reduction Potential Governs the Capacity of Quinones for Long-Distance Electron Transfer and Remote H2O2 Generation

Organic matter acts as a natural geobattery owing to the abundant rechargeable quinone moieties that span a large range of reduction potential (E_h). Here, we report that quinones’ E_h is a pivotal factor in determining their capacity to facilitate long-distance electron transfer and remote reactive oxygen species (ROS) generation. Among a series of quinone molecules with E_h from −0.50 to 0 V, quinones from E_h = −0.25 V to −0.14 V exhibit high efficiency to mediate long-distance electron transfer excreted by Shewanella oneidensis MR-1 for ROS generation. Mechanistic investigations show that quinones with E_h ≥ −0.25 V can act as terminal electron acceptors from microbial respiration. In-situ imaging results show that all reduced quinones could mediate electron transfer with a distance of 2.0–6.8 mm. Moreover, quinones with E_h ≤ −0.14 V could transfer carried electrons to oxygen molecules to generate ROS. Accordingly, 21.1% to 37.4% of redox-active moieties in aquatic and terrestrial organic matters were capable of efficiently mediating electron transfer from microbes to oxygen for ROS generation. We suggest that E_h distribution of organic matter is a pivotal parameter in the complex redox interactions between microbes, organic matter, and oxygen, thereby affecting biogeochemical processes in Earth’s surface systems.