The critical role of iron redox cycling in organic carbon dynamics of earthworm casts

Abstract

Earthworm casts are widely recognized as hotspots for soil organic carbon (SOC) cycling, commonly attributed to elevated microbial activity. However, the role of abiotic processes, specifically reactive iron (Fe) redox cycling, in SOC turnover within earthworm casts has not been fully explored. In this study, we collected earthworm casts and adjacent bulk soil, followed by a 90-day incubation experiment under controlled conditions. Our results showed that the reactive Fe(II) content in fresh earthworm casts was 5.53 times higher than in surrounding bulk soil. The elevated Fe(II) content facilitated the production of reactive oxygen species (ROS), with hydroxyl radical (•OH) contents reaching 3.34 times those in bulk soils. Quenching experiments demonstrated that ROS contributed to 26.9% of the initial CO2 emissions from fresh casts, highlighting the critical role of ROS in SOC mineralization. Meanwhile, Fe(II) oxidation promoted the accumulation of short-range ordered iron in cast, accompanied by a shift in organic matter stabilization from adsorption-dominated to co-precipitation-dominated mechanisms. Fourier transform ion cyclotron resonance mass spectrometry and thermodynamic analysis via substrate-explicit model analyses revealed that short-range ordered iron in aged casts preserved bioavailable organic matter-such as lipids, proteins and aminosugar-like compounds-thereby shielding them from rapid decomposition and promoting long-term stabilization. These findings uncover a previously unrecognized dual role of Fe redox cycling in earthworm casts: driving short-time OM mineralization through ROS and promoting OM stabilization via associations with Fe minerals. This study provides novel molecular-level evidence for iron-mediated abiotic–biotic coupling in SOC dynamics in agricultural soils.