Intensive culture of anecic earthworms (Amynthas aspergillum) under monoculture and coculture: impacts on vertical soil organic carbon accumulation via regulating microbial biomass and community structure in South China

• Intensive culture of anecic earthworms (ICAE) enhances soil carbon sequestration. • Earthworm monoculture increases SOC in 0–40 cm, while plant-earthworm coculture increases it across the 80 cm profile. • ICAE modulates POC content by regulating microbial biomass and community structure. • POC represents the key fraction driving MAOC enhancement and SOC accumulation in the ICAE system. • Coculture exhibits greater potential to promote SOC sequestration and microbial growth than monoculture. The effects of diversified agricultural management practices on soil organic carbon (SOC) have garnered increasing attention. However, intensive culture of anecic earthworms (ICAE) is a distinctive agricultural practice in South China that encompasses both monoculture and coculture systems, and its impacts on SOC content and fractions remains poorly understood. This study conducted a two-year field experiment with four treatments: Untreated control (C), a crop of trees Lonicera japonica (LJ), monoculture of earthworms Amynthas aspergillum (AA), and plant-earthworm coculture of L. japonica and A. aspergillum (LJ-AA). Contents and fractions of SOC, including mineral-associated organic carbon (MAOC) and particulate organic carbon (POC), were measured along the 0–80 cm soil profile. Additionally, soil pH, enzyme activities of peroxidase, polyphenol oxidase, β-D-glucosidase, and cellobiohydrolase, as well as the contents of phospholipid fatty acids, were analyzed to elucidate the mechanisms underlying ICAE-induced soil carbon sequestration. Results showed that compared to control, monoculture of A. aspergillum significantly increased the SOC content in the 0–40 cm soil profile by +61 to 77 %, while coculturing L. japonica and A. aspergillum increased SOC content of the whole 0–80 cm soil profile by +9.3 to 106 %. ICAE significantly increased total microbial biomass in the 0–20 cm soil layer, while reducing both the fungal-bacterial ratio and gram-positive to gram-negative bacterial ratio in the 60–80 cm layer. Additionally, ICAE significantly decreased peroxidase activity in the 60–80 cm soil layer, Polyphenol oxidase activity in the 20–40 cm soil layer, and β-D-glucosidase and cellobiohydrolase activities in the 40–60 cm and 60–80 cm soil layers. Partial least squares path analysis revealed that ICAE positively affected microbial biomass through direct action and indirect pH regulation, while negatively affecting community structure. Both microbial biomass and community structure mediated POC formation, which in turn facilitated MAOC accumulation. Finally, SOC accumulation occurred via POC and MAOC formation. In conclusion, ICAE promotes vertical SOC accumulation by regulating microbial biomass and community structure, and POC serves as the key fraction that drives MAOC enhancement and SOC accumulation. Notably, the coculture exhibits greater potential to promote SOC sequestration and microbial growth compared to monoculture, representing a more advantageous agricultural management system. To further validate the generalizability of these findings, future research should establish decadal-scale monitoring experiments and verify their applicability across diverse soil types and plant species.