Spatiotemporal dynamics of reactive oxygen species in the detritusphere and their critical roles in organic carbon mineralisation

Abstract

Reactive oxygen species (ROS) are recognised as important drivers of biogeochemical processes. However, the dynamics and distribution of ROS and their effects on carbon emissions in the detritusphere remain elusive. Herein, we visualised the production of ROS in situ (i.e. superoxide radical, O₂^•−; hydrogen peroxide, H₂O₂; and hydroxyl radical, ^•OH) in the detritusphere using a ROS-trapping agar gel, of which the contents gradually increased and then decreased with residue decay. Spatially, O₂^•− content gradually decreased with increasing distance from residue, whereas H₂O₂ content increased. Interestingly, the content of ^•OH increased from 3.2 to 4.3 μmol kg⁻¹ and decreased from 6.9 to 3.9 μmol kg⁻¹ with increasing distance from residue after incubation for 3 d and 24 d, respectively. Spearman correlation analysis revealed that O₂^•−production was closely related to the oxidation of water-soluble phenols by phenol oxidase. In contrast, H₂O₂ production correlated with microbial abundance, suggesting that microorganisms served as primary drivers of H₂O₂ production in the detritusphere. Results from incubation experiment suggest that the dominant drivers of ^•OH production shifted from Fe(II) to water-extractable organic carbon (WEOC) between day 3 and day 24 of residue decomposition. Furthermore, autoclaving reduced ^•OH content regardless of Fe(II) or WEOC presence, highlighting the important role of microorganism in ^•OH generation. The formed ROS significantly influenced the mineralisation of organic carbon (OC, P < 0.05), and the contributions varied by type of ROS. Specifically, ROS quenching experiments showed that ^•OH and O₂^•− stimulated OC mineralisation by 15% and 4%, respectively, while H₂O₂ reduced it by 18%. The obtained information highlights detritusphere as pervasive yet previously underestimated hotspots for ROS production, which has significant implication for soil OC mineralisation and priming effect.