Pioneer plants enhance soil multifunctionality by reshaping underground multitrophic community during natural succession of an abandoned rare earth mine tailing

Spontaneous natural succession in metal mine tailings is fundamental to the rehabilitation of bare tailing. Here, an abandoned rare earth element (REE) mine tailing with spontaneous colonisation by pioneer plants with different functional traits was selected. Soil nutrient cycling, fertility, organic matter decomposition as well as underground organismal communities and their multitrophic networks were investigated. Compared with the bare tailing, the colonisation with Lycopodium japonicum, Miscanthus sinensis, and Dicranopteris dichotoma increased soil multifunction by 222%, 293%, and 525%, respectively. This was accompanied by significant changes in soil bacterial and protistan community composition and increased soil multitrophic network complexity. Rhizospheres of different plant species showed distinct microbial community composition compared to that of bare tailing. Some WPS-2, Chloroflexi, and Chlorophyta were mainly present in the bare tailing, while some Proteobacteria and Cercozoa were predominantly seen in the rhizosphere. Pearson correlation and Random Forest revealed the biotic factors driving soil multifunction. Structural equation modelling further revealed that pioneer plants improved soil multifunction primarily by decreasing the microbial biodiversity and increasing the multitrophic network complexity. Overall, this highlights the importance of subterrestrial organisms in accelerating soil rehabilitation during natural succession and provides options for the ecological restoration of degraded REE mining areas. Environmental Implication This study elucidated the role of pioneer plants in promoting the recovery of soil multifunction based on plant-soil microbe interactions. The presence of vegetation at the mine tailings significantly increased soil multifunction. Rhizospheres of different plant species showed distinct bacterial and protistan microbial community composition compared to that of bare soil. Soil multifunction was regulated by soil bacterial and protistan biodiversity and soil multitrophic network complexity. This work highlights the importance of subterrestrial organisms in accelerating soil multifunctional recovery during spontaneous natural succession and provides options for the phytoremediation and soil management of degraded REE mining areas.