Hyphal tips actively develop strong adhesion with nutrient-bearing silicate to promote mineral weathering and nutrient acquisition

Abstract

Fungi actively enhance the local dissolution of nutrient-bearing minerals through the combined biomechanical and biochemical actions of their hyphal tips to obtain mineral-bound inorganic nutrients (MINs). However, little is known about the dynamic processes underlying hyphal tip-mineral interactions. Here, we assess the adhesive force between a single hypha of the common fungus Talaromyces flavus and the Fe-bearing silicate lizardite and quartz (as a control), as well as hyphal tip-induced lizardite weathering and hyphal Fe uptake. We showed that T. flavus hyphae formed their maximal adhesive force with lizardite at the growing tips, reaching 6.11 ± 0.69 nN after a contact time of one minute. The adhesive forces of the tip-lizardite interface within two minutes were >2.65 times stronger than those of the tip-quartz interface. Examination of the hyphal tip-lizardite interface after 18 h indicated the formation of dissolution channels with a depth of 27.7 ± 8.0 nm. Furthermore, the hyphal tips resulted in an altered lizardite up to 46 nm. The thickness of the altered lizardite increased to ∼130 nm after contact with the mature regions of the hyphae for ∼173 min. And the altered lizardite was found to have depleted Fe levels that increased with increasing contact time. The total content of Fe in T. flavus associated with the lizardite surface after 18 h was 52.98 ± 12.20 nmol mg−1, which was 6 times greater than the total amount of Fe in quartz surface-associated T. flavus after 24 h of culture. These results demonstrate that fungi access MINs by the active development of a strong adhesive force with target minerals through their hyphal tips, effectively enabling fungi to flourish in heterogeneous environments and be major geological agents for biogeochemical transformation.