Molecular mechanisms of iron nanominerals formation in fungal extracellular polymeric substances (EPS) layers during fungus-mineral interactions

Abstract

Extracellular polymeric substances (EPS), which envelop on fungal hyphae surface, interact strongly with minerals and play a crucial role in the formation of nanoscale minerals during biomineralization in nature environments. However, it remains poorly understood about the molecular mechanisms of nanominerals (i.e., iron nanominerals) formation in fungal EPS halos during fungus-mineral interactions. This process is vital because fungi typically grow attached to various mineral surfaces in nature. According to the changes of thickness of the fungal cell and EPS layers during the Trichoderma guizhouense NJAU 4742 and hematite cultivation experiments, we found that fungal biomineralization could trigger the formation of EPS layers. Fe-dominated nanominerals, aromatic C (283-286.1 eV), alkyl C (287.6-288.3 eV), and carboxylic C (288.4-289.1 eV) were the dominant chemical groups on the EPS layers, as determined by nanoscale secondary ion mass spectrometry (NanoSIMS), high-resolution transmission electron microscope (HRTEM), and carbon 1s near-edge X-ray absorption fine structure (NEXAFS) spectroscopy. Further, evidence from Fe K-edge X-ray absorption near-edge structure (XANES) and X-ray photoelectron spectroscopy (XPS) spectra indicated that oxygen vacancy (O_V) was formed on the Fe-dominated nanomineral surface during fungus-mineral interactions, which played an important role in catalyzing H₂O₂ decomposition and HO∗ production. Taken together, the intrinsic peroxidase-like activity by reactive oxygen species (ROS) could modulate the Fe-dominated nanominerals formation in EPS layers to newly form a physical barrier between the cell and the external environments around hyphae, providing novel insights into the effects of ROS-mediated fungal-mineral interactions on fungal nutrient recycling, attenuation of contaminants, and biological control in nature environments.