Surface lipids influence developmental and species-specific chemical signalling in nematodes

Abstract

ABSTRACT/SUMMARYChemical signalling facilitates organismal communication and coordinates physiological and behavioural processes. In nematodes, signalling has predominantly focused on secreted molecules leaving the surfaces communicative potential unexplored. By utilising 3D-OrbiSIMS, an advanced surface-sensitive mass spectrometry method, we directly characterised the molecular composition of the outermost regions (50 nm in depth) of Caenorhabditis elegans and Pristionchus pacificus to improve the understanding of surface-mediated chemical communication. We found that nematode surfaces consist of a lipid-dominated landscape (> 81 % C. elegans and > 69 % P. pacificus of all surveyed chemistries) with distinct compositions, which enrich in granularity and complexity through development. The surface-anchored lipids are also species-specific, reflecting evolutionary and ecological adaptations to their environmental niches. By exploring the effect of mutations on lipid production we found the peroxisomal fatty acid {beta}-oxidation component daf-22 is essential for defining the surface molecular fingerprint. This pathway is conserved across species in producing distinct chemical profiles, indicating its fundamental role in lipid metabolism and for maintaining surface integrity and function. Furthermore, we discovered that variations in surface-anchored lipids of C. elegans daf-22 larvae contribute to significantly increased susceptibility to predation by P. pacificus. Therefore, our findings reveal that the nematode surface is not just a passive boundary but a dynamic signalling platform with evolved, species-specific signatures. These molecular mechanisms are pivotal in shaping identity and communication strategies, providing new insights into the evolutionary and ecological dynamics of chemical signalling across organisms. HIGHLIGHTSO_LINematode surfaces are lipid-rich, changing with development. C_LIO_LISurface lipids are species-specific, reflecting adaptations. C_LIO_LIThe daf-22 gene is key in shaping the surface lipid profile. C_LIO_LISurface lipids mediate predator-prey interactions in nematodes. C_LI