In the laboratory C. elegans displays odor related behaviors such as attraction, aversion, and adaptation. Worms express vertebrate-like G-protein coupled odor receptors in the AWA and AWC olfactory sensory neurons to sense attractive odors that are thought to be important for tracking bacterial food sources. However culture conditions in the laboratory are vastly different than those C. elegans encounters in the wild. Recent studies have shown that C. elegans is densely populated in rotting fruit and vegetation, which can be a rich source of bacterial bonanzas for nematodes. We wondered whether C. elegans exploits olfactory behaviors to track bacteria in rotting fruit. Using a combination of food microbiology, biochemistry, behavioral analysis and genetics, we elucidate a possible predator-prey relationship between C. elegans and lactic acid bacteria (LAB) in rotting citrus fruit. LAB produces the volatile odor diacetyl as an oxidized by-product of fermentation in the presence of citrate, and we confirmed this using a colorometric assay to determine diacetyl production in LAB grown on citrate media or citrus fruit. We show that C. elegans is attracted to LAB only when grown on citrate media or yuzu fruit, a citrus fruit native to East Asia, but not other fruits or grains such as apple, tomato or barley malt. We show that the attraction to LAB is mediated by the diacetyl odor receptor, ODR-10. In addition, adaptation to diacetyl odor results in attenuation of attraction behavior to LAB grown on citrate. We isolated a wild LAB strain and a wild C. remanei strain from rotten yuzu collected from a farm. The wild LAB strain produces diacetyl when grown on citrate media or yuzu, and C. elegans attraction to the wild LAB grown on yuzu is mediated by ODR-10. We also demonstrate that the wild C. remanei is attracted to wild LAB when grown on citrate media or yuzu. These results not only identify an ecological function for a C. elegans olfactory behavior, but contribute to the growing understanding of the molecular and genetic basis for natural ecological phenomena.
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