Analysis of the Talaromyces flavus exometabolome reveals the complex responses of the fungus to minerals

Fungus-mineral interactions influence a variety of geochemical and biological processes on and near the Earth's surface. The secondary metabolites produced by fungi during these interactions control mineral weathering and affect geochemical element cycling; however, the extent to which minerals exert their influence on fungal metabolism has not been quantitatively determined in detail. Here, we used mass spectroscopy to investigate the exometabolome of Talaromyces flavus, a serpentine soil-inhabiting fungus, during interactions with antigorite, chlorite, hornblende, lizardite, magnetite, and quartz at 28 °C under aerobic conditions. Our experimental results showed that all the minerals used promoted spore germination and hyphal growth. The glucose consumption rate during the initial stages of the fungus-mineral interactions indicated that the metabolic activity of T. flavus was enhanced by a factor of ∼7 by lizardite, antigorite, chlorite, hornblende, and magnetite and by a factor of ∼3 by quartz. A total of 1198 secondary metabolites were detected at 166 h, and 977 (81.55%) of them were common to the T. flavus interactions with antigorite, chlorite, hornblende, lizardite, and magnetite. Statistical and comparative analyses of the 28 most common organic acids revealed that the production of these secondary metabolites by T. flavus was highly mineral-specific and that their content varied significantly in response to the different minerals. Moreover, the component composition of the secondary metabolites of T. flavus interacting with lizardite was more similar to chlorite and magnetite than to antigorite, hornblende, and quartz. Strong correlations were found between the production of gluconic, oxalic, citric, and itaconic acid and the bioavailability of certain elements. Fumaric and orsellinic acid production were stimulated by magnetite and chlorite, respectively. These results demonstrate that fungi can significantly regulate their metabolic behavior during interactions with minerals and that their metabolic regulation is primarily related to the chemical composition, weatherability, and surface properties of the minerals. Such biotic and abiotic responses have important implications for the fungus-induced geochemical transformation of minerals and metals.