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Published May 8, 2012 | Supplemental Material + Accepted Version
Journal Article Open

Ascaroside Signaling Is Widely Conserved among Nematodes

Abstract

Background: Nematodes are among the most successful animals on earth and include important human pathogens, yet little is known about nematode pheromone systems. A group of small molecules called ascarosides has been found to mediate mate finding, aggregation, and developmental diapause in Caenorhabditis elegans, but it is unknown whether ascaroside signaling exists outside of the genus Caenorhabditis. Results: To determine whether ascarosides are used as signaling molecules by other nematode species, we performed a mass spectrometry-based screen for ascarosides in secretions from a variety of both free-living and parasitic (plant, insect, and animal) nematodes. We found that most of the species analyzed, including nematodes from several different clades, produce species-specific ascaroside mixtures. In some cases, ascaroside biosynthesis patterns appear to correlate with phylogeny, whereas in other cases, biosynthesis seems to correlate with lifestyle and ecological niche. We further show that ascarosides mediate distinct nematode behaviors, such as retention, avoidance, and long-range attraction, and that different nematode species respond to distinct, but overlapping, sets of ascarosides. Conclusions: Our findings indicate that nematodes utilize a conserved family of signaling molecules despite having evolved to occupy diverse ecologies. Their structural features and level of conservation are evocative of bacterial quorum sensing, where acyl homoserine lactones (AHLs) are both produced and sensed by many species of gram-negative bacteria. The identification of species-specific ascaroside profiles may enable pheromone-based approaches to interfere with reproduction and survival of parasitic nematodes, which are responsible for significant agricultural losses and many human diseases worldwide.

Additional Information

© 2012 Elsevier Ltd. Received: December 14, 2011; Revised: February 16, 2012; Accepted: March 12, 2012; Published online: April 12, 2012. We thank the Caenorhabditis Genetics Center, Marie-Anne Felix, Antoon Ploeg, S. Patricia Stock, J. Scott Cameron, Teresa Mullens, Jennifer Becker, Scott Edwards, John Darsow, Adler R. Dillman, and Hillel T. Schwartz for their contribution of nematodes to this study. We further thank Adler R. Dillman for assembling a phylogenetic tree for the species used in this study. We thank Moises Garcia for his help in manufacturing the copper chambers used in the attraction assay. We thank Arthur S. Edison, Adler R. Dillman, Hillel T. Schwartz, Jagan Srinivasan, David A. Prober, and Bruce A. Hay for their valuable suggestions. This work was supported in part by a National Institutes of Health grant (GM088290 to F.C.S. and GM085285 to A.S. Edison, F.C.S., and P.W.S.), and the Howard Hughes Medical Institute, with which P.W.S. is an Investigator.

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Accepted Version - nihms365633.pdf

Supplemental Material - mmc1.pdf

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August 19, 2023
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