Earthworm activities change phosphorus mobilization and uptake strategies in deep soil layers

The drilosphere is described as a microbial hotspot in soil, which is rich in labile nutrients. However, phosphorus (P) quality and availability change along the drilosphere from labile organically-bound P in upper layers to immobilized Ca-phosphate with increasing depth. In this study, we postulated (1) that microbial P turnover is generally accelerated in the drilosphere compared to bulk soil as a result of an increase in labile nutrients, and (2) that P mineralization is dominant in upper layers of the drilosphere and P solubilization in deeper layers of the drilosphere, respectively. Furthermore, we hypothesized (3) that the enhanced P mobilization in the drilosphere favors copiotrophic and earthworm gut derived bacteria like Pseudomonadaceae, which distinguishes the community composition from that of the bulk soil. We investigated the effect of earthworm activities on potential phosphatase activities, abundance and diversity of bacterial communities involved in P mobilization (gcd, phoD, appA, phnX, phoN) and uptake (pstS, pitA) along a soil depth gradient in a short rotation coppice in Northeast Germany. Potential phosphatase activities and gene abundances revealed increasing potentials for organic P mineralization and high-affinity P uptake via the Pst system in the drilosphere below 50 cm depth. Conversely, in the upper soil layers potential for bacterial P mobilization were similar between drilosphere and bulk soil. We also observed drilosphere-related changes in the composition of bacterial communities involved in P solubilization and low-affinity P uptake via the Pit system below 60 cm depth. In the drilosphere compared to bulk soil, Pseudomonadaceae were enriched and played a major role in solubilization and low-affinity uptake of P, while bacteria potentially involved in N turnover like Bradyrhizobiaceae and Phyllobacteriaceae were less abundant. Our study suggested that earthworms increased the potential enzyme activity and abundance of bacteria carrying the Pho-regulon genes in the drilosphere of the deeper soil layers. Furthermore, earthworm-derived bacteria were enriched in the drilosphere at the same soil depth, especially those involved in P solubilization and carrying the Pit system.