Abstract

BackgroundDispersal 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), e.g., Steinernema feltiae. Regulation of dispersal behavior has not been thoroughly investigated for C. elegans or any other nematode species. Based on the fact that ascarosides regulate entry in dauer stage as well as multiple behaviors in C. elegans adults including mating, avoidance and aggregation, we hypothesized that ascarosides might also be involved in regulation of dispersal behavior in C. elegans and for other nematodes such as IJ of phylogenetically related EPNs.Methodology/Principal FindingsLiquid 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.Conclusions/SignificanceAscaroside blends represent evolutionarily conserved, fundamentally important communication systems for nematodes from diverse habitats, and thus may provide sustainable means for control of parasitic nematodes.

Highlights

  • Entomopathogenic nematodes (EPN), such as Heterorhabditis spp. and Steinernema spp. are obligate insect parasites that kill and consume their hosts with the aid of symbiotic bacteria [1]

  • Dispersal assay For entomopathogenic nematodes (EPN), insect cadavers are known to promote dispersal behavior of the infective juveniles (IJ) stage [20]

  • Liquid chromatography-mass spectrometry (LC-MS) analyses of the cadaver extract revealed the presence of an ascaroside [15] supporting the hypothesis that S. feltiae might utilize ascarosides as dispersal signals

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Summary

Introduction

Entomopathogenic nematodes (EPN), such as Heterorhabditis spp. and Steinernema spp. are obligate insect parasites that kill and consume their hosts with the aid of symbiotic bacteria [1]. When the conditions are not favorable for normal growth and development, such as high temperature, high density, or low food availability, it forms dauer larvae (alternative 3rd larvae) This specialized life stage, which does not feed and is resistant to stressful conditions [4,5,6], is analogous to IJs of entomopathogenic nematodes and second stage juveniles (J2) of plant parasitic root-knot nematodes [7]. 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), e.g., Steinernema feltiae. Based on the fact that ascarosides regulate entry in dauer stage as well as multiple behaviors in C. elegans adults including mating, avoidance and aggregation, we hypothesized that ascarosides might be involved in regulation of dispersal behavior in C. elegans and for other nematodes such as IJ of phylogenetically related EPNs

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