ARS | Publication request: Interspecific nematode signals regulate dispersal behavior

Submitted to: PLoS One
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: May 2, 2012
Publication Date: June 6, 2012
Citation: Kaplan, F., Alborn, H.T., Von Reuss, S.H., Ajredini, R., Ali, J.G., Akyazi, F., Stelinski, L.L., Edison, A.S., Schroeder, F.C., Teal, P.E. 2012. Interspecific nematode signals regulate dispersal behavior. PLoS One. 7(6):1-8.

Interpretive Summary: For many organisms, dispersal is an important behavior for survival. During conditions unfavorable for growth and development, the free living bacteriovorus nematode Caenorhabditis elegans produces stress resistant and food seeking dispersal larvae, called dauer. This stage is analogous to the plant infective second stage juveniles (J2) of plant parasitic nematodes as well as infective juveniles (IJ)s of insect parasitic nematodes, eg. Steinernema feltiae. Despite the agricultural importance of these nematode life stages, regulation of dispersal has not been thoroughly investigated for any nematode species. Based on recently identified C. elegans pheromones, called ascarosides, scientists at USDA ARS CMAVE in Gainesville Florida in collaboration with scientists at University of Florida and Cornell University, hypothesized that related compounds also might be involved in regulation of dispersal. Four known ascarosides were found in a strongly dispersal inducing C. elegans dauer conditioned media. The dispersal could be mimicked by a synthetic blend even in the presence of food. The blend also induced dispersion of IJs of S. feltiae and J2s of plant parasitic Meloidogyne spp. Assay guided fractionation revealed structural analogs as major active components of the S. feltiae and C. elegans dispersal blends. In addition, all analyzed Steinernema spp. and Heterorhabditis spp. infected insect host cadavers turned out to have one major ascaroside in common. We propose that ascaroside blends represent evolutionarily conserved and fundamentally important communication systems for many nematodes species that can provide sustainable means for control of parasitic nematodes.

Technical Abstract: Dispersal is an important nematode behavior. Upon crowding or food depletion, the free living bacteriovorus nematode Caenorhabditis elegans produces stress resistant dispersal larvae, called dauer, which are analogous to second stage juveniles (J2) of plant parasitic Meloidogyne spp. and infective juveniles (IJ)s of entomopathogenic nematodes (EPN), eg. Steinernema feltiae. Regulation of dispersal behavior has not been thoroughly investigated for C. elegans or any other nematode species. Similar to EPNs, the free living bacteriovor Caenorhabditis briggsae can infect and develop within insect larvae, which also is the case for C. elegans when raised with C. briggsae associated bacteria. This suggests that Caenorhabditis spp. and phylogenetically related EPNs may utilize similar signaling molecules. Based on previously identified blends of ascarosides regulating mating behavior in C. elegans, we hypothesized that ascarosides might also be involved in regulation of dispersal behavior. Liquid chromatography-mass spectrometry analysis of C. elegans dauer conditioned media, which shows strong dispersing activity, revealed four known ascarosides (ascr#2, ascr#3, ascr#8, icas#9). A synthetic blend of these ascarosides at physiologically relevant concentrations dispersed C. elegans dauer in the presence of food and also caused dispersion of IJs of S. feltiae and J2s of plant parasitic Meloidogyne spp. Assay guided fractionation revealed structural analogs as major active components of the S. feltiae (ascr#9) and C. elegans (ascr#2) dispersal blends. Further analysis revealed ascr#9 in all Steinernema spp. and Heterorhabditis spp. infected insect host cadavers. Ascaroside blends represent evolutionarily conserved, fundamentally important communication systems for nematodes from diverse habitats, and thus may provide sustainable means for control of parasitic nematodes.