Chemical imaging reveals phosphorus mobilization patterns in earthworm-engineered drilosphere

Abstract

Earthworms are soil ecosystem engineers who play a crucial role in phosphorus (P) cycling, encompassing inorganic P desorption and organic P mineralization. Although the role of earthworms in P mobilization is well documented, the spatial distribution of P mobilization processes and critical microbial species within the earthworm-engineered soil microhabitat, known as the drilosphere, remains to be determined. This study investigated P mobilization and redistribution in the drilosphere by ex situ chemical analyses, in situ soil zymography and diffusive gradients in thin-films imaging, and assessment of the microorganism communities. Endogeic earthworm species Metaphire guillelmi was incubated for 30 days in pots filled with soils Fluvisol or Acrisol with different total P contents (0.6 and 1.2 mg kg⁻¹, respectively). Chemical analyses revealed that total P content in earthworm casts increased by 120 % in Fluvisol and 7.7 % in Acrisol. Available P content increased by 8.5 times in Fluvisol and 4.4 times in Acrisol in the drilosphere compared to bulk soil due to elevated acid/alkaline phosphatase activities and intensified Fe/Al-bound P desorption amongst others. Imaging identified co-existing and distinct hotspots for available P and acid phosphatase activity in soils surrounding the burrow walls, with hotspot proportions of 0.1 %‒3.1 % and 5.4 %‒7.5 % of the imaged areas. Earthworm activity increased the abundance of specific bacterial (Aeromonas and Flavobacterium) and fungal (Scedosporium and Podospora) taxa potentially contributing to P mobilization. The correlation between the distribution of metal-bound adsorption sites, phosphatase activity, and diffusion mechanisms contributed to the available P redistribution in the soil. These findings provide insights for developing soil management strategies that harness earthworm-mediated P cycling to optimize nutrient use efficiency and reduce external P inputs in sustainable agricultural systems.