Accelerated microbial activity, turnover and efficiency in the drilosphere is depth dependent

Anecic earthworms such as Lumbricus terrestris create effective channels for the translocation of organic substances, nutrients (N, P) and water between top- and subsoil. However, studies on localized and linked microbial activities with the biochemical mechanisms within drilosphere are missing. To clarify the enzymatic mechanisms, zymography was combined with 14C imaging by placing 14C-labeled wheat litter on the surface of mesocosms with top- and subsoil to feed earthworms. Cellobiohydrolase and acid phosphatase activities were compared in drilosphere and bulk soil to test two hypotheses: i) a positive spatial correlation between 14C images and enzyme activities at burrow edges reflects the interactions between substrate distribution and microbial activities; ii) the drilosphere has higher enzyme activities and faster substrate turnover compared to bulk soil independent on depth. In line with the first hypotheses, the localization of substrates (14C) overlapped with enzyme activities for 68%. Spatial distribution of enzyme activities had stronger gradients within 2 mm of burrow edges in topsoil and 4 mm in subsoil. The mineralization of the wheat litter was faster in drilosphere than in the bulk soil. In contrast to our second hypothesis, the substrate turnover was depth dependent: 14CO2 efflux was fourfold faster in topsoil than subsoil drilosphere. The decline of enzyme activities with depth, accompanied by decreasing catalytic efficiency, implies microbial production of more efficient enzymes in top-than in the subsoil. We conclude that interactions between enzymes and substrates are more tight in the drilosphere, making it microbial hotspots. Thus, earthworm activities lead to microbial localization and acceleration of litter decomposition and C turnover in drilosphere. Therefore, both direct hotspot and indirect (soil heterogeneous content) effects need to be explicitly considered when attempting to model and predict how bioturbation evens will alter ecosystem dynamics and ecological development of (micro)habitats.