Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey
Yen-Ping Hsueh,
Matthew R Gronquist,
Erich M Schwarz,
Ravi David Nath,
Ching-Han Lee,
Shalha Gharib,
Frank C Schroeder,
Paul W Sternberg
Affiliations
Yen-Ping Hsueh
Division of Biology and Biological Engineering, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, United States; Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan
Matthew R Gronquist
Department of Chemistry, State University of New York at Fredonia, Fredonia, United States
Erich M Schwarz
Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States
Ravi David Nath
Division of Biology and Biological Engineering, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, United States
Ching-Han Lee
Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan
Shalha Gharib
Division of Biology and Biological Engineering, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, United States
Frank C Schroeder
Boyce Thompson Institute, Cornell University, Ithaca, United States; Department of Chemistry and Chemical Biology, Cornell University, Ithaca, United States
To study the molecular basis for predator-prey coevolution, we investigated how Caenorhabditis elegans responds to the predatory fungus Arthrobotrys oligospora. C. elegans and other nematodes were attracted to volatile compounds produced by A. oligospora. Gas-chromatographic mass-spectral analyses of A. oligospora-derived volatile metabolites identified several odors mimicking food cues attractive to nematodes. One compound, methyl 3-methyl-2-butenoate (MMB) additionally triggered strong sex- and stage-specific attraction in several Caenorhabditis species. Furthermore, when MMB is present, it interferes with nematode mating, suggesting that MMB might mimic sex pheromone in Caenorhabditis species. Forward genetic screening suggests that multiple receptors are involved in sensing MMB. Response to fungal odors involves the olfactory neuron AWCs. Single-cell RNA-seq revealed the GPCRs expressed in AWC. We propose that A. oligospora likely evolved the means to use olfactory mimicry to attract its nematode prey through the olfactory neurons in C. elegans and related species.
