Chemical imaging reveals phosphorus mobilization patterns in earthworm-engineered drilosphere

• Soil zymography and DGT chemical imaging tools were applied to the drilosphere. • Phosphatase activity and labile P hotspots were identified using chemical imaging. • Spatial P heterogeneity in the drilosphere was intensified by earthworm activities. • Earthworm bioturbation altered microbial community structure and boosted P mobility. • Earthworm-mediated P mobilization occurred both via epidermal mucus and cast pathways. 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.

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Publication Details

Journal
Geoderma
Published
2025-09-01
DOI
https://doi.org/10.1016/j.geoderma.2025.117497
Citations
1
Primary Topic
Phosphorus and nutrient management
Type
article
Field-Weighted Citation Impact
1.00
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Chemical imaging reveals phosphorus mobilization patterns in earthworm-engineered drilosphere

Yvan Capowiez, Jia-Lu Gao, Zhen-Yu Qiang, Q. Lena et al.
1 citations
Geoderma
Phosphorus and nutrient management
1.00
article

Chemical imaging reveals phosphorus mobilization patterns in earthworm-engineered drilosphere

Yvan Capowiez, Jia-Lu Gao, Zhen-Yu Qiang, Q. Lena, Anna Gunina, Dong‐Xing Guan, Daniel Menezes‐Blackburn, Gang Li
article en
1 citations

Abstract

• Soil zymography and DGT chemical imaging tools were applied to the drilosphere. • Phosphatase activity and labile P hotspots were identified using chemical imaging. • Spatial P heterogeneity in the drilosphere was intensified by earthworm activities. • Earthworm bioturbation altered microbial community structure and boosted P mobility. • Earthworm-mediated P mobilization occurred both via epidermal mucus and cast pathways. 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.

GeodermaVol. 461
Chinese Academy of Sciences (CN), Université d'Avignon et des Pays de Vaucluse (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Institute of Applied Ecology (CN), Institute of Urban Environment (CN), ZheJiang Academy of Agricultural Sciences (CN), Sultan Qaboos University (OM), Ostwestfalen-Lippe University of Applied Sciences and Arts (DE)
Openalex Percentile: Top 19%
Phosphorus and nutrient management
1.00
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