22Microbe-mineral interactions have shaped the surface of the Earth and impacted the evolution of 23 plants and animals. Although more than two-thirds of known mineral species have biological 24 imprints, how the biotransformation of minerals may have benefited microbial development, 25 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 towards understanding the feedback pathways controlling the evolution of biogenic mineral formation. 40 41 42 KEYWORDS 43 4 microbe-mineral interactions, biomineralization, fungi, iron acquisition, nanoparticles, nanozymes, oxidative stress, surface oxygen anions, geomycology 45 nanoparticles were obtained from TEM imaging and particle-size distribution analysis using

Fungal-mediated extracellular reactive oxygen species (ROS) are essential for biogeochemical cycles of carbon, nitrogen, and contaminants in terrestrial environments. These ROS levels may be modulated by iron nanoparticles that possess intrinsic peroxidase (POD)-like activity (nanozymes). However, it remains largely undescribed how fungi modulate the POD-like activity of the iron nanoparticles with various crystallinities and crystal facets. Using well-controlled fungal–mineral cultivation experiments, here, we showed that fungi possessed a robust defect engineering strategy to modulate the POD-like activity of the attached iron minerals by decreasing the catalytic activity of poorly ordered ferrihydrite but enhancing that of well-crystallized hematite. The dynamics of POD-like activity were found to reside in molecular trade-offs between lattice oxygen and oxygen vacancies in the iron nanoparticles, which may be located in a cytoprotective fungal exoskeleton. Together, our findings unveil coupled POD-like activity and oxygen redox dynamics during fungal–mineral interactions, which increase the understanding of the catalytic mechanisms of POD-like nanozymes and microbial-mediated biogeochemical cycles of nutrient elements as well as the attenuation of contaminants in terrestrial environments.

Summary Fungal–mineral interactions can produce large amounts of biogenic nano‐size (~ 1–100 nm) minerals, yet their influence on fungal physiology and growth remains largely unexplored. Using Trichoderma guizhouense NJAU4742 and magnetite (Mt) as a model fungus and mineral system, we have shown for the first time that biogenic Mt nanoparticles formed during fungal–mineral cultivation exhibit intrinsic peroxidase‐like activity. Specifically, the average peroxidase‐like activity of Mt nanoparticles after 72 h cultivation was ~ 2.4 times higher than that of the original Mt. Evidence from high resolution X‐ray photoelectron spectroscopy analyses indicated that the unique properties of magnetite nanoparticles largely stemmed from their high proportion of surface non‐lattice oxygen, through occupying surface oxygen‐vacant sites, rather than Fe redox chemistry, which challenges conventional Fenton reaction theories that assume iron to be the sole redox‐active centre. Nanoscale secondary ion mass spectrometry with a resolution down to 50 nm demonstrated that a thin (< 1 μm) oxygen‐film was present on the surface of fungal hyphae. Furthermore, synchrotron radiation‐based micro‐FTIR spectra revealed that surface oxygen groups corresponded mainly to organic OH, mineral OH and carbonyl groups. Together, these findings highlight an important, but unrecognized, catalytic activity of mineral nanoparticles produced by fungal–mineral interactions and contribute substantially to our understanding of mineral nanoparticles in natural ecosystems.

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