A Mineral-Doped Micromodel Platform Demonstrates Fungal Bridging of Carbon Hot Spots and Hyphal Transport of Mineral-Derived Nutrients.

Soil fungi facilitate the translocation of inorganic nutrients from soil minerals to other microorganisms and plants. This ability is particularly advantageous in impoverished soils because fungal mycelial networks can bridge otherwise spatially disconnected and inaccessible nutrient hot spots. However, the molecular mechanisms underlying fungal mineral weathering and transport through soil remains poorly understood primarily due to the lack of a platform for spatially resolved analysis of biotic-driven mineral weathering. Here, we addressed this knowledge gap by demonstrating a mineral-doped soil micromodel platform where mineral weathering mechanisms can be studied. We directly visualize acquisition and transport of inorganic nutrients from minerals through fungal hyphae in the micromodel using a multimodal imaging approach. We found that Fusarium sp. strain DS 682, a representative of common saprotrophic soil fungus, exhibited a mechanosensory response (thigmotropism) around obstacles and through pore spaces (~12 μm) in the presence of minerals. The fungus incorporated and translocated potassium (K) from K-rich mineral interfaces, as evidenced by visualization of mineral-derived nutrient transport and unique K chemical moieties following fungus-induced mineral weathering. Specific membrane transport proteins were expressed in the fungus in the presence of minerals, including those involved in oxidative phosphorylation pathways and the transmembrane transport of small-molecular-weight organic acids. This study establishes the significance of a spatial visualization platform for investigating microbial induced mineral weathering at microbially relevant scales. Moreover, we demonstrate the importance of fungal biology and nutrient translocation in maintaining fungal growth under water and carbon limitations in a reduced-complexity soil-like microenvironment.