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: 9.92). 04/2012; 22(9):772-80. DOI: 10.1016/j.cub.2012.03.024
Source: PubMed

ABSTRACT 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.

  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Dispersal processes are known to influence dynamics of marine benthic communities. It has been argued that as a result of nematodes being small in size and lacking pelagic larvae, it is unlikely that they are able to dis-perse actively over wide geographical ranges. Nematode dispersal is therefore assumed to be predominantly driven by water currents entraining resuspended sediments containing nematodes. Three different types of substrates combined with sediment (algae, bacteria, and sulphides) and two different controls (empty and azoic sediment) were offered to a nematode community sinking through the water column in three indepen-dent, simultaneously running replicated experiments. Selective settlement of nematodes was observed whilst descending in the water column under ex-situ experimental conditions using samples collected in the Whittard canyon at 812 m of water depth. Significant differences in nematode community structure be-tween treatments suggest that different nematodes are attracted by different substrates. They may colonise suitable patches selectively when descending in the water column, but whether they are attracted by food or by other attractants, such as pheromones or other chemical signals, is still unclear. High abundances of the chemosynthetic, mouthless nematode Astomonema found in the canyon study area over medium-scale distances (10–100 m) contribute to the idea that resuspension events enable dispersal of nematodes over larger distances, after which active settlement can occur through chemical attraction.
    Journal of Experimental Marine Biology and Ecology 03/2013; 441:110-116. DOI:10.1016/j.jembe.2013.01.021 · 2.48 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Nematodes use an extensive chemical language based on glycosides of the dideoxysugar ascarylose for developmental regulation (dauer formation), male sex attraction, aggregation, and dispersal. However, no examples of a female- or hermaphrodite-specific sex attractant have been identified to date. In this study, we investigated the pheromone system of the gonochoristic sour paste nematode Panagrellus redivivus, which produces sex-specific attractants of the opposite sex. Activity-guided fractionation of the P. redivivus exometabolome revealed that males are strongly attracted to ascr#1 (also known as daumone), an ascaroside previously identified from Caenorhabditis elegans hermaphrodites. Female P. redivivus are repelled by high concentrations of ascr#1 but are specifically attracted to a previously unknown ascaroside that we named dhas#18, a dihydroxy derivative of the known ascr#18 and an ascaroside that features extensive functionalization of the lipid-derived side chain. Targeted profiling of the P. redivivus exometabolome revealed several additional ascarosides that did not induce strong chemotaxis. We show that P. redivivus females, but not males, produce the male-attracting ascr#1, whereas males, but not females, produce the female-attracting dhas#18. These results show that ascaroside biosynthesis in P. redivivus is highly sex-specific. Furthermore, the extensive side chain functionalization in dhas#18, which is reminiscent of polyketide-derived natural products, indicates unanticipated biosynthetic capabilities in nematodes.
    Proceedings of the National Academy of Sciences 12/2012; DOI:10.1073/pnas.1218302109 · 9.81 Impact Factor
  • Acarologia 12/2014; 54(4):371-394. DOI:10.1051/acarologia/20142144