Nematode-Trapping Devices of Arthrobotrys oligospora is an Iron Storage Phenotype Adapted to Temperature Changes

Abstract

The discovery of eukaryotes exhibiting an iron overload phenotype holds significant implications for developing treatments and strategies for human iron overload diseases caused by genetic defects. Under low-nutrient conditions, Arthrobotrys oligospora and other nematode-trapping fungi (NTF) can differentiate their mycelia into specialized structures for capturing prey as their nutritional source. Recent work has indicated that siderophore deficiency exacerbates the discrepancies between trapping device development and fungal carnivorous activity in A. oligospora, which has long been thought to represent a degeneration of the fungal carnivorous capacity. Using transmission electron microscopy combined with 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 peroxisome development in the mycelia. Importantly, the characteristic electron-dense bodies in trapping devices store more iron compared to vacuoles and mitochondria. Genomic analysis indicated that NTFs lack the pivotal CccA-mediated vacuolar iron detoxification pathway that is conserved in most fungi. A Bayesian relaxed molecular clock analysis suggested that the evolutions of NTFs coincided with global warming. We demonstrated that the trapping devices of A. oligospora, triggered by high temperatures, can act as a system to sequester excess iron, thereby preventing abnormal free iron contents in mycelia and helping the fungi adapt to hot environments. Our findings reveal a non-trophic environmental factor that triggers iron overload and a diagnostic phenotypic indicator of iron overload in eukaryotes. This suggests that NTFs could serve as a potential eukaryotic model for elucidating the mechanisms of dynamic regulation of iron homeostasis, which could aid in treating iron overload-induced diseases in humans.