Nematode-trapping fungus Arthrobotrys oligospora is hungry for iron-chelating agent COQ7 of nematodes

Iron homeostasis is critical for the survival of almost all organisms, yet its dysregulation is often caused by a synergistic effect of genetic and environmental factors. Previous studies have shown that trapping devices of the predominant nematode-trapping fungus (NTF) Arthrobotrys oligospora serve as an unprecedented iron sequestration system compensatory for lack of the crucial fungal vacuolar iron detoxification mechanism. Here, we found that among the Ascomycota phylum, only NTFs lacked gene coq7, which encodes COQ7 responsible for ubiquinol (UQ) biosynthesis and efficient iron chelation. Addition of exogenous UQ₁₀ or heterologous expression of yeast gene coq7 in A. oligospora inhibited the formation of fungal trapping devices. Interestingly, mutant nematodes with disruption of gene coq7 can greatly reduce nematode-capturing ability of fungal trapping devices. Exogenous COQ7s exhibit significant adsorption effects on fungal trapping devices both in vitro and in vivo. Transcriptional, metabolic, mutational, and phenotypic analyses indicated that A. oligospora utilized a chemotaxonomic class of highly oxygenated arthrobotrisins with similar characteristics to UQ₃, instead of UQs, in response to elevated oxygen levels. Loss of arthrobotrisin biosynthesis led to a delayed growth of the mutant Δart but enhanced UQ₈ biosynthesis, trapping device formation, and nematicidal activity. Time-calibrated evolutionary analyses, combined with geological data, indicated that the NTF ancestor lost the coq7 gene after acquiring the art gene cluster during the cold "superoligotrophy" period, characterized by dramatic shifts in global oxygen levels and temperature changes. Our findings indicated that the trapping devices of NTF capture nematodes primarily for iron chelation therapy, rather than solely for food, which addresses the long-standing issue regarding the limited carnivorous ability of trapping devices.