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 (Eh). Here, we report that quinones' Eh 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 Eh from -0.50 to 0 V, quinones from Eh = -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 Eh ≥ -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 Eh ≤ -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 Eh 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.