Surface Lipids in Nematodes are Influenced by Development and Species-specific Adaptations

Kotowska, Anna M.; Hiramatsu, Fumie; Alexander, Morgan R.; Scurr, David J.; Lightfoot, James W.; Chauhan, Veeren M.

Abstract

The surface of an organism is a dynamic interface that continually adapts to its environment. In nematodes, the cuticle forms a complex boundary that protects against the physicochemical pressures. However, the precise molecular composition and function of this surface remain largely unexplored. By utilizing 3D-OrbiSIMS, an advanced surface-sensitive mass spectrometry method, we directly characterized the molecular composition of the outermost regions (∼50 nm) of Caenorhabditis elegans and Pristionchus pacificus to improve the understanding of species-specific surface lipid composition and its potential roles in nematode biology. 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 lipids are also species-specific, potentially highlighting distinct molecular compositions that are derived from diverging evolutionary paths. By exploring the effect of mutations on lipid production, we found the peroxisomal fatty acid β-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 maintaining the surface integrity and function. Furthermore, we discovered that variations in surface lipids of C. elegans daf-22 larvae contribute to significantly increased susceptibility to predation by P. pacificus. Therefore, our findings reveal that nematode surface lipids are developmentally dependent, species-specific, and fundamental in interspecies interactions. These insights pave the way for further exploration into the physiological and behavioral significance of surface lipids.

Citation

Kotowska, A. M., Hiramatsu, F., Alexander, M. R., Scurr, D. J., Lightfoot, J. W., & Chauhan, V. M. (2025). Surface Lipids in Nematodes are Influenced by Development and Species-specific Adaptations. Journal of the American Chemical Society, 147(8), 6439-6449. https://doi.org/10.1021/jacs.4c12519

• Journal Article Type: Article
• Acceptance Date: Jan 17, 2025
• Online Publication Date: Feb 12, 2025
• Publication Date: Feb 26, 2025
• Deposit Date: Mar 28, 2025
• Publicly Available Date: Mar 28, 2025
• Journal: Journal of the American Chemical Society
• Print ISSN: 0002-7863
• Electronic ISSN: 1520-5126
• Publisher: American Chemical Society
• Peer Reviewed: Peer Reviewed
• Volume: 147
• Issue: 8
• Pages: 6439-6449
• DOI: https://doi.org/10.1021/jacs.4c12519
• Keywords: Cluster ions, Ions, Lipids, Mass spectrometry, Surface chemistry
• Public URL: https://nottingham-repository.worktribe.com/output/45436589
• Publisher URL: https://pubs.acs.org/doi/10.1021/jacs.4c12519