Fungal Nanophase Particles Catalyze Iron Transformation for Oxidative Stress Removal and Iron Acquisition

Abstract

Microbe-mineral interactions have shaped the surface of the Earth and impacted the evolution of plants and animals. Although more than two-thirds of known mineral species have biological imprints, how the biotransformation of minerals may have benefited microbial development, beyond nutritional and energetic use, remains enigmatic. In this research, we have shown that biogenic ferrihydrite nanoparticles are extensively formed at the interface between an actively growing fungus and an iron-containing mineral, hematite. These biogenic nanoparticles formed through the fungus-hematite interactions can behave as mimetic catalysts, similar to nanozymes that imitate peroxidase, which scavenges hydrogen peroxide for the mitigation of potential cytotoxicity. Evidence from various X-ray spectroscopic analyses indicated that non-lattice oxygen in the nanomaterials was chiefly responsible for this catalytic activity, rather than through the conventional mechanisms of iron redox chemistry. Cryo-scanning electron microscopy, high-resolution (∼30nm) 3D volume rendering, and biomass analyses further confirmed that the organism was active and capable of mediating the catalytic reactions. We therefore hypothesize that this confers an advantage to the organism in terms of protection from oxidative stress and ensuring the acquisition of essential iron. This work raises new questions about the roles of biogenic nanomaterials in the coevolution of the lithosphere and biosphere and provides a step toward understanding the feedback pathways controlling the evolution of biogenic mineral formation.