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Abstract:
Nematodes are the most abundant animal in the soil ecosystem, where they cohabitate with an array of natural predators including insects, other nematodes and nematophagous fungi. Considering the prevalence and abundance of nematodes, it is not surprising that multiple groups of fungi have independently evolved the ability to switch to a predatory lifestyle on nematodes under nutrient deprivation. Among these carnivorous fungi, the nematode-trapping fungus Arthrobotrys oligospora is one of the most ubiquitous and well-studied species. This emerging model species develops adhesive nets as a trapping device to capture its nematode prey. Multiple conserved signaling pathways, such as the cAMP and the MAPK pathways, have been shown to play a role in prey-sensing and trap morphogenesis. However, little is known about how the traps capture nematodes. To dissect the molecular basis of the robust adhesion between nematodes and fungal traps, we conducted forward genetic screens in Caenorhabditis elegans to identify mutants capable of escaping from A. oligospora traps. Genetic mapping and whole genome sequencing of seven such mutants revealed that loss-of-function mutations in a nuclear hormone receptor gene, nhr-66, resulted in resistance to A. oligospora predation. Since nuclear hormone receptors are transcription factors that function as master regulators, we conducted RNAseq analysis on wild-type and nhr-66 mutant animals and found that more than 60 collagen genes were down-regulated in the nhr-66 mutants. Overexpression of the down-regulated collagen genes in the nhr-66 mutant abolished the escape phenotype, revealing that collagens play a crucial role in mediating adhesion between fungal traps and nematode prey. Interestingly, we have not identified loss-of-function nhr-66 variants in wild C. elegans populations. This result suggests that there is a fitness trade-off for possessing an nhr-66 mutation and that the adhesins on the fungal traps likely recognize multiple targets on the nematode surface, showcasing the evolutionary arms race between nematode-trapping fungi and their nematode prey.
