Ascaroside Signaling Is Widely Conserved among Nematodes

Howard Hughes Medical Institute and Biology Division, California Institute of Technology, 1200 E. California Boulevard, Pasadena, CA 91125, USA.
Current biology: CB (Impact Factor: 9.57). 04/2012; 22(9):772-80. DOI: 10.1016/j.cub.2012.03.024
Source: PubMed


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.
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.
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.

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Available from: Robin B Gasser, Feb 11, 2014
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    • "Dauer larva formation assays were carried out as previously described [16] with all assays using 30 mm diameter plates containing with 2 mL of dauer agar [16,20]. Each dauer agar plate was inoculated with 20 μL of 2 or 5% food (w/v) of E. coli OP50 [24], onto which five hermaphrodites of similar age were introduced and allowed to lay eggs for a period of 3-4 hours or until approximately 50 eggs were present on each plate, after which the hermaphrodites were removed. "
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    ABSTRACT: Animals use environmental information to make developmental decisions to maximise their fitness. The nematode Caenorhabditis elegans measures its environment to decide between arresting development as dauer larvae or continuing to grow and reproduce. Worms are thought to use ascarosides as signals of population density and this signalling is thought to be a species-wide honest signal. We compared recently wild C. elegans lines' dauer larva arrest when presented with the same ascaroside signals and in different food environments. We find that the hitherto canonical dauer larva response does not hold among these lines. Ascaroside molecules can, depending on the food environment, both promote and repress dauer larva formation. Further, these recently wild C. elegans lines also produce ascaroside mixtures that induce a wide diversity of dauer larva formation responses. We further find that the lines differ in the quantity and ratios of ascaroside molecules that they release. Some of the dauer larva formation responses are consistent with dishonest signalling. Together, the results suggest that the idea that dauer larva formation is an honestly-signalled C. elegans-wide effect does not hold. Rather, the results suggest that ascaroside-based signalling is a public broadcast information system, but where the correct interpretation of that information depends on the worms' context, and is a system open to dishonest signalling.
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    • "The C. elegans dauer develops under stressful conditions such as overcrowding by sensing dauer and other ascaroside pheromones, signal transduction through insulin and TGF-β pathways and DAF-12 nuclear hormone receptor [57]–[63]. H. bacteriophora produces an ascaroside ethanolamine (C11 EA) derivative that maintains the IJ state at high IJ densities and additional ascarosides [64], [65]. We found that H. bacteriophora has most (19 of 23) of the insulin/IGF-1 signaling pathway genes that are critical for dauer formation and for regulation of longevity, stress resistance and innate immunity in C. elegans (Figure 2). "
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    • "Although a chemical attraction over medium and large distances (metres to kilometres) would be improbable , pheromones could act as an attractant in the settling process of nematodes. In this experiment, the offered Petri-dish substrates did not contain any nematodes, but chemical signalling by the first settlers cannot be excluded as an aid to selective settlement (Choe et al., 2012). Patterns in chemotaxis are already clear for some groups, such as the annelid Protodrilus rubropharyngeus, which is positively attracted to bacteria (Gray, 1967) and blue crabs (Callinectes sapidus), which employ their chemical senses to forage, but for the meiofauna this is still unclear (Zimmer and Butman, 2000). "
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