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Abstract:
Nutritional deprivation triggers a saprotrophic to predatory lifestyle switch in soil dwelling nematode-trapping fungi (NTF). In particu- lar, Arthrobotrys oligospora has evolved to secrete food and sex cues to lure their prey – Nematoda animals – 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 Caenorhabditis elegans. A dynamic transcriptomic reaction that indicated a strong reliance on protein secretion was observed. A comprehensive prediction of the secretome of A. oligospora resulted in 1084 transcripts, 64% of which 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 early time point, 2hr-post C. elegans exposure, suggesting that the TOR signaling pathway might be critical for sensing the presence of nematodes. Rapamycin treatment inhibited both trap development and function. Moreover, a plasma membrane t-SNARE protein, SSO2, involved in membrane fusion of secretory vesicles, plays a major role in nematode-adhesion. We subsequently predicted the putative effectors of A. oligospora and found that they represent approximately 19% of the secretome and that their expression peaked after 10 hours of introduction of nematodes. Specifically, we found that genes of the Egh16 family were highly upregulated upon nematode exposure. In situ hybridization reveals the accumulation of the top three highly expressed Egh16 transcripts in the traps cell. Thus, we named these gene family as Trap-enriched Secreted Protein (TSP). Gene deletion of the highest expressed gene TSP1 impairs the function of trap. Lastly, Egh16 gene family is highly expanded in the genomes of several nematode-trapping fungi, suggesting that this gene family may have a critical role for the evolution of the predatory life style in Ascomycetes.
