Soil Chemical Properties, Metabolome, and Metabarcoding Give the New Insights into the Soil Transforming Process of Fairy Ring Fungi Leucocalocybe mongolica

A unique ecological landscape distributed in the Mongolian Plateau, called fairy rings, caused by the growth of the fungus Leucocalocybe mongolica (LM) in the soil could promote plant growth without fertilization. Therefore, this landscape can alleviate fertilizer use and has excellent value for agricultural production. The previous studies only investigated several parameters of the fairy rings, such as soil microbial diversity and some soil chemical properties, thus conclusions based on the studies on fairy rings lack comprehension. Therefore, the present study systematically investigated the chemical properties, metabolome, and metabarcoding of LM-transformed soil. We analyzed fairy ring soils from DARK (FR) and OUT (CK) zone correlated growth promotion with ten soil chemical properties, including N, nitrate-N, inorganic-P, cellulose, available boron, available sulfur, Fe, Mn, Zn, and Cu, which were identified as important markers to screen fairy ring landscapes. Metabolomics showed that the accumulation of 17 carbohydrate-dominated metabolites was closely associated with plant growth promotion. Finally, metabarcoding detected fungi as the main components affecting soil conversion. Among the various fungi at the family level, Lasiosphaeriaceae, unidentified_Auriculariales_sp, and Herpotrichiellaceae were markers to screen fairy ring. Our study is novel and systematically reveals the fairy ring soil ecology and lists the key factors promoting plant growth. These findings lay a theoretical foundation for developing the fairy ring landscape in an agricultural system.