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

TY - JOUR

T1 - Fungal Nanophase Particles Catalyze Iron Transformation for Oxidative Stress Removal and Iron Acquisition

AU - Yu, Guang-Hui

AU - Chi, Zhi-Lai

AU - Kappler, Andreas

AU - Sun, Fu-Sheng

AU - Liu, Cong-Qiang

AU - Teng, Hui Henry

AU - Gadd, Geoffrey Michael

N1 - This work was supported by the National Natural Science Foundation of China (grant nos. 41977271, 41830859, 41972041, and 11227902). G.M.G. gratefully acknowledges research support of the Geomicrobiology Group from the Natural Environment Research Council, UK (NE/M010910/1 and NE/M 011275/1).

PY - 2020/8/3

Y1 - 2020/8/3

N2 - 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 (∼30 nm) 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.

AB - 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 (∼30 nm) 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.

KW - microbe-mineral interactions

KW - biomineralization

KW - fungi

KW - iron acquisition

KW - nanoparticles

KW - nanozymes

KW - oxidative stress

KW - surface oxygen anions

KW - geomycology

KW - catalysis

U2 - 10.1016/j.cub.2020.05.058

DO - 10.1016/j.cub.2020.05.058

M3 - Article

C2 - 32531287

SN - 0960-9822

VL - 30

SP - 1-8.e1-e4

JO - Current biology : CB

JF - Current biology : CB

ER -