Fungus-mineral interactions play unparalleled roles in shaping the planet Earth but are underappreciated relative to bacterial influences. Unique to fungus, but largely unknown, are the interfacial processes and extensiveness of hypha- versus spore-mineral interactions given the associated turgor pressure differences and the vast contact areas between mycelia and minerals in the critical zone. Here we examine lizardite [Mg3Si2O5(OH)4] dissolution by single cells of a native fungal strain using confocal laser scanning microscopy, atomic force microscopy, and transmission electron microscopy–energy dispersive X-ray spectroscopy to explore the mechanism, driving force, and magnitude of the interfacial reactions. Results from our inspection showed (1) significant pH reduction in the vicinity of cells upon mineral surface attachment, (2) exclusive Fe loss from the mineral at the cell-mineral interfaces, and (3) destruction of the mineral crystal structure below the area colonized by hyphae but not that by spores. Compared to the results from bulk experiments and at the mineral-water interface, these observations indicate that (1) only attached cells release siderophores and (2) biomechanical forces of hyphal growth are indispensable for fungal weathering and strong enough to breach the mineral lattice. Estimated mineral mass loss at the interface suggests that cellular dissolution can ultimately account for ∼40%–50% of the overall bio-weathering, significantly larger than the previous estimate of ∼1% contribution.