Differential microbial roles in the organic layer and mineral soil determine radioactive cesium fate in forest ecosystems.

Radioactive cesium (137Cs) contamination poses a long-term ecological challenge, particularly in forest ecosystems. While 137Cs is known for its persistence, the role of soil microorganisms in determining its fate remains insufficiently understood. This study presents a dynamic assessment of microbial 137Cs retention, focusing on the complex interplay among microorganisms, organic matter, and clay minerals within the organic layer-mineral soil system. Using time-series sampling, chloroform fumigation-extraction, and DNA sequencing, we tracked changes in microbial 137Cs retention over eight years following the Fukushima Daiichi Nuclear Power Plant accident. Our results show that rapid microbial recycling contributes to sustaining a potentially bioavailable 137Cs pool in the organic layer, thereby facilitating 137Cs recycling between the layer and plants. This microbial involvement rapidly diminishes as 137Cs activity concentrations in the organic layer decline due to leaching into the mineral soil. In the mineral soil, minimal microbial 137Cs retention was observed, suggesting an indirect microbial role in facilitating 137Cs immobilization by clay minerals through organic matter decomposition. Bacterial and fungal community compositions differed between the organic layer and topsoil. Notably, microbial 137Cs retention in the organic layer is regulated by 137Cs availability, independent of region, forest type, and time since deposition. These findings provide a unified explanation for observed differences in 137Cs persistence in organic layers between European and Japanese forests and refine our understanding of microbial contributions to radionuclide biogeochemistry. The insights have broader implications for ecological risk assessment beyond the Fukushima disaster.