Predation, in which individuals of one species (predators) kill and consume the biomass of individuals of another species (prey) (Abrams, 2000), imposes a strong selective pressure on both predators and prey. To minimize the risk of being eaten, prey have often evolved specific behaviors and strategies such as camouflage, avoidance, mimicry, and tonic immobility to increase their chance of survival. In turn, predators also evolved enhanced predatory strategies to secure food sufficient to survive and reproduce, giving rise to an evolutionary arms race between predator and prey (Dawkins and Krebs, 1979).
While most carnivores are animals, examples of predacious plants and fungi exist. Venus flytraps, sundews and pitcher plants acquire some or most of their nutrients from trapping and consuming insects, a feature that evolved in response to nitrogen limitation (Darwin, 1875). Many fungi that grow in nitrogen-poor environments have likewise evolved carnivorism and nematodes, being the most numerically abundant animals on earth, conveniently became the prey (Barron, 1977; Nordbring-Hertz, 1988). This predatory lifestyle has independently evolved multiple times among different fungal lineages including Zygomycetes, Ascomycetes and Basidiomycetes (Barron, 1977; Liou and Tzean, 1997; Yang et al., 2007). Nematode-trapping fungi depend on their elaborate traps to prey on nematodes. However, the majority of the nematode-trapping fungi do not constitutively generate these trapping structures; trap-morphogenesis is only triggered by the presence of nematodes (Pramer and Stoll, 1959). This suggests that trap-formation might be a highly energy-consuming process and that, to conserve energy, these fungi have evolved to sense signals from nematodes, which indicate the presence of prey. One such signal is the group of nematode pheromones, ascarosides. These pheromones regulate various aspects of behavior and development in C. elegans and are sufficient to induce trap-morphogenesis in several species of nematode-trapping fungi (Hsueh et al., 2013). Since the nematode-trapping fungi have clearly evolved the ability to eavesdrop on nematode communication, we wondered whether the nematodes also sense and respond to their fungal predators.
C. elegans is known to respond to pathogenic bacteria. For example, Pseudomonas aeruginosa triggers an aversive learning behavior, while another pathogen Bacillus nematocida attracts C. elegans (Niu et al., 2010; Zhang et al., 2005). Bacterial secondary metabolites are able to modulate the signaling and the protective lawn-avoidance behavior in C. elegans, demonstrating that the sensory neurons of C. elegans are critical for its defensive responses against pathogens (Meisel et al., 2014; Pradel et al., 2007; Zhang et al., 2005). By contrast, little is known about how C. elegans responds to its natural predators such as the nematode-trapping fungi, with only an early study showing that the nematode Panagrellus redivivus was attracted to a species of nematode-trapping fungi (Balan and Gerber, 1972). Many prey are known to begin fleeing when they sense a possible predator, while many predators are also known to attract their prey (Haynes et al., 2002; Rosier, 2011). Therefore, we investigated the behavioral and molecular basis for how C. elegans responds to Arthrobotrys oligospora, one of the most common nematode-trapping fungal species and one that we had previously found to eavesdrop on ascarosides produced by C. elegans (Hsueh et al., 2013).
Here, we show that C. elegans and other nematodes are attracted to A. oligospora and the attraction observed for C. elegans is mediated by the two AWC olfactory neurons. We identified several odorants produced by A. oligospora and found that many of the odorants attracted C. elegans, and appear to represent olfactory mimics of the food and sex cues. Through genetic screens and single-cell transcriptome analyses of the AWC neuron, we identified the potential chemosensory receptors that were expressed in this neuron, which is involved in sensing some of these fungal odors. Our study shows that in order to catch its nematode prey, A. oligospora has evolved to lure the nematodes by producing olfactory mimicry of the food and sex cues that are attractive to Caenorhabditis nematodes.
