Bespoke strategies of Paxillus involutus to extract potassium from diverse phyllosilicates

Phyllosilicates provide a primary source of minerals used by microorganisms and plants, particularly clay minerals, i.e., phyllosilicates of very small particle size. Fungi can actively break down (or "weather") minerals to extract nutrients, but whether they use identical mechanisms when accessing different clay minerals is unclear. In addition, it is yet to be understood whether starvation stresses due to the limited availability of a mineral-nutrient would result in different weathering behaviours of microbes. Here, we performed a microcosm experiment to address these questions. We used the ectomycorrhizal basidiomycete Paxillus involutus and the phyllosilicates K-vermiculite, muscovite and phlogopite. These silicates have different degrees of recalcitrance to the removal of K cations from the mineral, and each was provided in the microscosm experiment as the sole potassium (K) source. The type of potassium "extraction-assimilation" was tested against a potassium-availability gradient, with a situation of maximum starvation stress (no potassium availability) and one of maximum availability (potassium provided as a solute in the culture medium). Our study revealed that different phyllosilicate minerals stimulated different patterns of fungal gene expression, which indicated bespoke weathering mechanisms for different phyllosilicates. The potassium uptake capacity of the fungus was highest with K-vermiculite compared to phlogopite and muscovite. Interestingly, the assimilation of phosphorus by the fungus was reduced in K-depleted conditions. Moreover, the potassium deprivation condition prompted the fungus to assimilate sodium instead. Also, in the presence of the minerals, the fungus showed significant differences in gene expression compared with the negative and positive control conditions, suggesting that the mineral environment modulates the starvation stress levels. The nutrients assimilated by the mycelium from both the minerals and the culture medium also varied according to the type of silicate added and the K starvation level to which the fungus was subjected. Based on what has been observed here, many geochemical processes could depend on fungi's genetic and functional plasticity, which would have considerable environmental consequences with a direct link between the evolution of fungi and that of the Earth's crust.