Soil microbial interkingdom interactions are critical to microbial resiliency under water and nutrient stress. Within soil microbiomes, fungal constituents are believed to be among the most successful under water and nutrient limited conditions. This is partly due to the filamentous hyphal networks of most soilborne fungi, which permit them to link and exploit discrete substrate pools. Furthermore, widespread fungal interactions with plants and bacteria make fungi integral to all aspects of C, N, P, and S cycling within soil. Nonetheless, the precise mechanisms by which soil fungi sense and access specific nutrient sources under drought remain vastly understudied. Here, we explored the role of fungal hyphal networks in soil under drought-like conditions by use of a controlled soil environment (SoilBox). The SoilBox enables determination of the spatial organization and metabolic interactions between members of soil microbial communities by use of optical and mass spectrometry imaging techniques. Subsequently, we applied soil micromodels, which simulate the porosity and mineralogy of soil, to determine how a specific soil fungus, Fusarium chlamydosporum reacted to limited soil moisture conditions. In general, this research provided a deeper mechanistic insight into the processes that govern mycelial bridging of nutrient sources within the soil microenvironment.
Results/Conclusions
Within the SoilBox, we were able to visualize fungal hyphal networks bridging disparate chitin islands over distances of 27 mm in soil under limited soil moisture conditions. The multimodal imaging results showed chitin island decomposition by the native soil microbial community under different moisture regimes, where degradation of the islands was not significantly altered under dry soil conditions in comparison to soil moisture at field capacity (under the timeframe measured, days). Within the soil micromodels, we observed increased hyphal density and fungal thigmotropism around obstacles and through pore spaces when the micromodels were enhanced with minerals. Mass spectrometry imaging showed cation enrichment and translocation in fungal hyphae grown in mineral-enhanced micromodels. Translocation from minerals by hyphae resulted in K+ speciation (via X-ray near edge absorption analysis). Conversely, mycelia grown in native micromodels did not exhibit thigmotropic behavior, micronutrient cation translocation, or K+ speciation. These results provide direct evidence of hyphal translocation of micronutrients from a mineral surface under nutrient limiting conditions. Combined, these studies demonstrate that mycelial acquisition and transport of mineral-derived inorganic nutrients provides fungal communities a survival advantage under water limited conditions, where they can access discrete nutrient pools within soil microenvironments and act as nutrient highways.