Chemical imaging reveals phosphorus mobilization patterns in earthworm-engineered drilosphere
Zhen-Yu Qiang,
Dong-Xing Guan,
Jia-Lu Gao,
Gang Li,
Daniel Menezes-Blackburn,
Anna Gunina,
Yvan Capowiez,
Lena Q. Ma
Affiliations
Zhen-Yu Qiang
State Key Laboratory of Soil Pollution Control and Safety, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China
Dong-Xing Guan
State Key Laboratory of Soil Pollution Control and Safety, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China; Corresponding author.
Jia-Lu Gao
State Key Laboratory of Soil Pollution Control and Safety, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China
Gang Li
State Key Laboratory of Regional and Urban Ecology, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China
Daniel Menezes-Blackburn
Department of Soils, Water and Agricultural Engineering, CAMS, Sultan Qaboos University, PO Box 34, Al-khod 123, Sultanate of Oman
Anna Gunina
Department of Soil Biogeochemistry, OWL University of Applied Sciences and Arts, Lippe 37671, Germany; Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
Yvan Capowiez
INRAE, UMR1114, EMMAH, INRAE/Université d’Avignon, Site Agroparc, 84914 Avignon cedex 09, France
Lena Q. Ma
State Key Laboratory of Soil Pollution Control and Safety, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China
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.
