Global gene transcription and metabolite secretion during hydroxyapatite solubilisation by the ectomycorrhizal fungus Paxillus involutus in symbiosis with Pinus silvestris
Ectomycorrhizal fungi form symbiotic partnerships with tree roots and are able to biochemically weather inorganic phosphorus (Pi)-rich minerals such as apatites and provide Pi to their host in return for photosynthates. Fungal-driven nutrient cycling based on mineral weathering plays a critical role in ecosystem and crop productivity and geochemical cycling. However, the transcriptional responses to symbiosis and weathering of mineral phosphates in ectomycorrhizal fungal hyphae are largely unknown. An artificial system was developed to study the solubilisation of hydroxyapatite by P. involutus. This was confirmed by EDX spectroscopy data, which showed depletion of Pi from the HAP crystals along with the formation of secondary minerals. RNA-seq analysis revealed that ectomycorrhizal symbiosis induced a different set of genes in the hyphae of P. involutus than in the non-symbiotically growing fungus, including specific expression of organic acid metabolism genes. Metabolomic analysis using UPLC-Q-TOF-MS led to the identification of several secreted metabolites enriched in the presence of hydroxyapatite in P. involutus systems growing non-symbiotically or in symbiosis with P. sylvestris seedlings. The analysis also led to the identification of novel metabolic compounds secreted during the weathering process. The results of the transcriptome and metabolome analyses were combined to create a mechanistic model of HAP weathering by P. involutus at the molecular level