Fungal strategies of potassium extraction from silicates of different resistance as manifested in differential weathering and gene expression

The environmental availability of mineral nutrients plays a role in the adaptation and evolution of soil fungi and fungus-plant symbiotic systems. As nutrient availability is different from soil to soil, it is expected that the most adapted fungi can express multiple genes to promote different mechanisms of mineral attack and of metabolic routes to maximize the use of nutrient resources at the lowest energy cost. Microcosm experiments of Paxillus involutus growing on muscovite, phlogopite and K-exchanged vermiculite as K sources were carried out for 21 days. Gene expression analysis indicated that the level of K-deprivation stress was muscovite > phlogopite ≫ K-vermiculite. Genes and functions overexpressed in the experiments indicated meaningful metabolic activities including K extraction and transport. SEM-EDS and micro-XRD (∼1.15 mm resolution) analysis of mineral surfaces and chemical analysis of agar and mycelium indicated weathering processes and K uptake in good agreement with gene expression analysis. In many areas, P. involutus caused physical damage to the minerals without any apparent chemical attack, consisting of tracks of different depth, from <1 μm to ∼80 μm wide, and piles of removed material. However, all minerals were partly dissolved. Phlogopite and vermiculite presented cation-depleted areas, but not muscovite. The dissolution trends of phlogopite and vermiculite were similar, with loss of K, Al and Mg, and concentration of Si, Ti and Fe, although Si and Fe were also lost with respect to Ti. The different mobilization of Al and Fe is noteworthy. Release of K from vermiculite by cation exchange was extensive, both abiotic and driven by P. involutus. The experimental conditions closest to most environmental situations are those in K-vermiculite tests. The results provide a new and coherent insight into fungal adaptation to mineral nutrient stress where fungal activity was regulated by both K requirement and success of the actions to secure it.