Mineral foraging and etching by the fungus Talaromyces flavus to obtain structurally bound iron

Abstract

Fungi possess remarkable abilities to acquire mineral nutrients through foraging for and weathering minerals, and these fungal behaviors are influenced by the physiochemical properties of the minerals. Here, we investigated the dynamic processes underlying these behaviors in the interactions between the common fungus Talaromyces flavus and two serpentine minerals (antigorite and lizardite) and quartz as a control. In the culture of T. flavus on solid Czapek medium with these minerals, we found that the elongation rates of T. flavus hyphae toward antigorite and lizardite particles were similar, and both were much higher than those toward quartz particles. After reaching the minerals, the growth of T. flavus was promoted significantly by antigorite and lizardite. Atomic force microscopy measurements uncovered the production of distinct dissolution channels with a depth of 29.34 ± 6.18 nm on the lizardite surface, but no local dissolution was found on the antigorite surface. Laser ablation multicollector inductively coupled plasma mass spectrometric analysis indicated that the total Fe in T. flavus hyphae grown on the surfaces of lizardite and antigorite flakes was ~8.3 and 2.3 times, respectively of those grown on the surface of medium. Whewellite was ubiquitously found at the hyphal tips and their vicinity during T. flavus interactions with lizardite. These results demonstrate that fungal hyphae have a remarkable capacity to sense and respond to minerals and to extract structurally bound inorganic nutrients, and highlight that the instant weathering of minerals by fungi represents an important but unassessed contributor to the short-term release of mineral nutrients and should be incorporated into biogeochemical models.