Abstract
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.
Highlights
Predation, in which individuals of one species kill and consume the biomass of individuals of another species (Abrams, 2000), imposes a strong selective pressure on both predators and prey
A. oligospora cultures were grown in two quadrants of a plate, following which synchronized adult C. elegans were placed in the middle of the plates and allowed to crawl freely until they reached a source of sodium azide in each quadrant that paralyzed the worms (Figure 1A)
We found that the adult C. elegans were consistently attracted to A. oligospora, suggesting that the fungus might lure the worms by producing compounds that are attractive to them (Figure 1B)
Summary
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. 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
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