Nematode-Trapping Devices of Arthrobotrys oligospora is an Iron Storage System Mediated by Elevated Temperatures

Under low-nutrient conditions, nematode-trapping fungi (NTFs) can differentiate their mycelia into specialized trapping devices for capturing prey. Using energy-dispersive X-ray spectroscopy (EDX) in conjunction with transmission electron microscopy (TEM), together with a series of bioassay, we identified that the characteristic electron-dense bodies in trapping devices contained more iron than vacuoles and mitochondria, functioning as an unrecognized iron storage organelle. Genomic analysis revealed that all NTFs lack the Ccc1-mediated vacuolar iron detoxification mechanism conserved in most fungi. Heterogenous expression of yeast-derived Ccc1 gene in A. oligospora significantly reduced trapping device formation and nematicidal activity. Mapping key factor fluctuations onto Bayesian relaxed molecular clock analysis indicated that the loss of Ccc1-mediated vacuolar iron storage occurred during Late Paleozoic Ice Age, whereas the emergence of trapping devices and the acquisition of desferriferrichrome were closely associated with elevated temperatures. Temperature bioassays showed that trap formation is highly temperature-dependent, with free iron levels inversely correlated with temperature, consistent with the temperature sensitivity of A. oligospora, which cannot grow above 30 °C. Our findings demonstrated that global temperature fluctuations serve as a critical driver of the evolution of NTFs and act as a catalyst for the emergence of trapping devices, novel phenotypic indicator of eukaryotic iron overload.