Trapping Devices of Carnivorous fungus Arthrobotrys oligospora is a Phenotypic System for Separating Thermally-Induced Excess Irons

The discovery of eukaryotes with an iron overload phenotype offers promising insights for developing treatments and strategies for human iron overload diseases caused by genetic defects. Under nutrient-limited conditions, Arthrobotrys oligospora and other nematode-trapping fungi (NTF) can differentiate their mycelia into specialized structures to capture prey as a nutritional source. Recent work has shown that siderophore deficiency worsens the discrepancies between trapping device development and fungal carnivorous activity in A. oligospora, previously believed to indicate a degeneration of its carnivorous capacity. Using transmission electron microscopy, energy-dispersive X-ray spectroscopy, and functional analyses, we identified siderophore-deficient mutants that develop numerous trapping devices but lack a significant number of iron-containing ferrichrome granules and exhibit autophagosomes in their mycelia. Notably, the electron-dense bodies in trapping devices store more iron than vacuoles and mitochondria. Genomic analysis revealed that NTFs lack the crucial CccA-mediated vacuolar iron detoxification pathway, which is conserved in most fungi. Bayesian relaxed molecular clock analysis suggested that the evolution of NTFs coincided with global warming. We demonstrated that the trapping devices of A. oligospora, triggered by high temperatures, function as a system to sequester excess iron, thus preventing abnormal free iron levels in mycelia and aiding the fungi in adapting to hot environments. Our findings identify a non-trophic environmental factor that triggers iron overload and a phenotypic indicator of iron overload in eukaryotes. This suggests that NTFs could serve as a potential eukaryotic model for elucidating the dynamic regulation mechanisms of iron homeostasis, potentially aiding in the treatment of iron overload-induced diseases in humans.