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Interspecific nematode signals regulate dispersal behavior.

Kaplan F, Alborn HT, von Reuss SH, Ajredini R, Ali JG, Akyazi F, Stelinski LL, Edison AS, Schroeder FC, Teal PE - PLoS ONE (2012)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Center for Medical, Agricultural and Veterinary Entomology, Agricultural Research Service, United States Department of Agriculture (USDA-ARS), Gainesville, Florida, United States of America. fkaplan@ufl.edu

ABSTRACT

Background: 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), 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 findings: 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.

Conclusions/significance: 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.

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Related in: MedlinePlus

Dispersal assay.(A) Naturally dispersing infective juveniles (IJ) of S. feltiae from an insect cadaver. (B) Approximately 300 IJs were placed on an agar plate in water. (C) IJs were treated with either water (control) or insect cadaver extract. Images are representative of six experiments for each treatment. (D) Dispersal assay on the same plate. The illustration represents two experiments. Behavior is temperature and season dependent. Assays were conducted at RT (22±0.5°C) or under temperature controlled conditions.
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pone-0038735-g001: Dispersal assay.(A) Naturally dispersing infective juveniles (IJ) of S. feltiae from an insect cadaver. (B) Approximately 300 IJs were placed on an agar plate in water. (C) IJs were treated with either water (control) or insect cadaver extract. Images are representative of six experiments for each treatment. (D) Dispersal assay on the same plate. The illustration represents two experiments. Behavior is temperature and season dependent. Assays were conducted at RT (22±0.5°C) or under temperature controlled conditions.

Mentions: 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]. C. elegans is typically found in decomposing plant material [2], [3]. It completes its life cycle within 3.5 days under standard laboratory conditions. 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]. (Meloidogyne spp) that are equally adapted to survive conditions unfavorable for normal growth and development. Upon depletion of food resources or when overcrowded, infectious juveniles (IJs) of entomopathogenic nematodes and dauer larvae of the free living nematode Caenorhabditis elegans display a dispersal behavior [4], [8]. This is demonstrated by highly mobile EPNs, Steinernema feltiae IJs, leaving a host cadaver (Fig 1A and Movie S1).


Interspecific nematode signals regulate dispersal behavior.

Kaplan F, Alborn HT, von Reuss SH, Ajredini R, Ali JG, Akyazi F, Stelinski LL, Edison AS, Schroeder FC, Teal PE - PLoS ONE (2012)

Dispersal assay.(A) Naturally dispersing infective juveniles (IJ) of S. feltiae from an insect cadaver. (B) Approximately 300 IJs were placed on an agar plate in water. (C) IJs were treated with either water (control) or insect cadaver extract. Images are representative of six experiments for each treatment. (D) Dispersal assay on the same plate. The illustration represents two experiments. Behavior is temperature and season dependent. Assays were conducted at RT (22±0.5°C) or under temperature controlled conditions.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368880&req=5

pone-0038735-g001: Dispersal assay.(A) Naturally dispersing infective juveniles (IJ) of S. feltiae from an insect cadaver. (B) Approximately 300 IJs were placed on an agar plate in water. (C) IJs were treated with either water (control) or insect cadaver extract. Images are representative of six experiments for each treatment. (D) Dispersal assay on the same plate. The illustration represents two experiments. Behavior is temperature and season dependent. Assays were conducted at RT (22±0.5°C) or under temperature controlled conditions.
Mentions: 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]. C. elegans is typically found in decomposing plant material [2], [3]. It completes its life cycle within 3.5 days under standard laboratory conditions. 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]. (Meloidogyne spp) that are equally adapted to survive conditions unfavorable for normal growth and development. Upon depletion of food resources or when overcrowded, infectious juveniles (IJs) of entomopathogenic nematodes and dauer larvae of the free living nematode Caenorhabditis elegans display a dispersal behavior [4], [8]. This is demonstrated by highly mobile EPNs, Steinernema feltiae IJs, leaving a host cadaver (Fig 1A and Movie S1).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Center for Medical, Agricultural and Veterinary Entomology, Agricultural Research Service, United States Department of Agriculture (USDA-ARS), Gainesville, Florida, United States of America. fkaplan@ufl.edu

ABSTRACT

Background: 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), 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 findings: 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.

Conclusions/significance: 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.

Show MeSH
Related in: MedlinePlus