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Molecular Trade-Offs between Lattice Oxygen and Oxygen Vacancy Drive Organic Pollutant Degradation in Fungal Biomineralized Exoskeletons

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posted on 2022-05-13, 20:03 authored by Zhi-Lai Chi, Guang-Hui Yu, H. Henry Teng, Hai-Gang Liu, Jian Wang, Cong-Qiang Liu, Qi-Rong Shen, Geoffrey Michael Gadd
Fungal–mineral interactions can effectively alleviate cellular stress from organic pollutants, the production of which are expected to rapidly increase owing to the Earth moving into an unprecedented geological epoch, the Anthropocene. The underlying mechanisms that may enable fungi to combat organic pollution during fungal–mineral interactions remain unclear. Inspired by the natural fungal sporulation process, we demonstrate for the first time that fungal biomineralization triggers the formation of an ultrathin (hundreds of nanometers thick) exoskeleton, enriched in nanosized iron (oxyhydr)­oxides and biomolecules, on the hyphae. Mapped biochemical composition of this coating at a subcellular scale via high spatial resolution (down to 50 nm) synchrotron radiation-based techniques confirmed aromatic C, C–N bonds, amide carbonyl, and iron (oxyhydr)­oxides as the major components of the coatings. This nanobiohybrid system appeared to impart a strong (×2) biofunctionality for fungal degradation of bisphenol A through altering molecular-level trade-offs between lattice oxygen and oxygen vacancy. Together, fungal coatings could act as “artificial spores”, which enable fungi to combat physical and chemical stresses in natural environments, providing crucial insights into fungal biomineralization and coevolution of the Earth’s lithosphere and biosphere.