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Abstract:
Nutritional deprivation triggers a saprotrophic to predatory lifestyle switch in soil dwelling nematode-trapping fungi (NTF). In particular, Arthrobotrys oligospora has evolved to secrete food and sex cues to lure their nematode prey into an adhesive network of traps, specialized structures that originate from the vegetative mycelium. Upon capture, the nematodes are invaded and digested by the fungus, thus serving as a food source. We employed RNA-sequencing to examine the response of A. oligospora upon exposure to the model nematode Caenorhabdi- tis elegans. A dynamic transcriptomic reaction that indicated a strong reliance on protein secretion was observed. Two-thirds of the predict- ed secretome of A. oligospora are upregulated in the presence of C. elegans at all tested time points. We found a large number of genes related to ribosome biogenesis induced at an early time point, suggest- ing that the TOR signaling pathway might be critical. Moreover, a plas- ma membrane t-SNARE protein, SSO2, involved in membrane fusion of secretory vesicles, plays a major role in nematode-adhesion. We sub- sequently predicted the putative effectors of A. oligospora and found that they represent approximately 19% of the secretome. Specifically, we found that genes of the Egh16 family were highly upregulated upon nematode exposure and highly expanded in the genomes of several NTF, suggesting a role for the evolution of the predatory lifestyle in Ascomycetes. In situ hybridization and GFP fusion protein reveals the accumulation of the highly expressed Egh16 in the traps cell. Thus, we named these gene family as Trap Enriched Protein (TEP). Gene dele- tion of the highest expressed gene TEP1 impairs the function of traps. Lastly, upregulation of the serine and metalloproteases were observed during the nematode digestion process. Protease inhibitors thwart fun- gal infection after penetration, demonstrating that proteases facilitate hyphal growth and prey digestion.
