Targeted metabolomics reveals a male pheromone and sex-specific ascaroside biosynthesis in Caenorhabditis elegans.
In the model organism Caenorhabditis elegans, a class of small molecule signals called ascarosides regulate development, mating, and social behaviors. Ascaroside production has been studied in the predominant sex, the hermaphrodite, but not in males, which account for less than 1% of wild-type worms grown under typical laboratory conditions. Using HPLC-MS-based targeted metabolomics, we show that males also produce ascarosides and that their ascaroside profile differs markedly from that of hermaphrodites. Whereas hermaphrodite ascaroside profiles are dominated by ascr#3, containing an α,β-unsaturated fatty acid, males predominantly produce the corresponding dihydro-derivative ascr#10. This small structural modification profoundly affects signaling properties: hermaphrodites are retained by attomole-amounts of male-produced ascr#10, whereas hermaphrodite-produced ascr#3 repels hermaphrodites and attracts males. Male production of ascr#10 is population density-dependent, indicating sensory regulation of ascaroside biosynthesis. Analysis of gene expression data supports a model in which sex-specific regulation of peroxisomal β-oxidation produces functionally different ascaroside profiles.
Boyce Thompson Institute and Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853, USA.
Yevgeniy
Y
Izrayelit
Jagan
J
Srinivasan
Sydney L
SL
Campbell
Yeara
Y
Jo
Stephan H
SH
von Reuss
Margaux C
MC
Genoff
Paul W
PW
Sternberg
Frank C
FC
Schroeder
D000818:Animals; D001522:Behavior, Animal; D017173:Caenorhabditis elegans; D002633:Chemotaxis; D002851:Chromatography, High Pressure Liquid / Q000379:methods; D005227:Fatty Acids / Q000737:chemistry; D005231:Fatty Acids, Unsaturated / Q000378:metabolism; D005786:Gene Expression Regulation; D006027:Glycosides / Q000737:chemistry; D008297:Male; D013058:Mass Spectrometry / Q000379:methods; D055432:Metabolomics / Q000379:methods*; D008954:Models, Biological; D020675:Peroxisomes / Q000378:metabolism; D010675:Pheromones / Q000737:chemistry*; D015398:Signal Transduction
D005227:Fatty Acids; D005231:Fatty Acids, Unsaturated; D006027:Glycosides; D010675:Pheromones