Habitat shapes the lipidome of the tropical photosynthetic sea slug Elysia crispata

Abstract

Sacoglossan sea slugs have attracted considerable scientific attention due to their capacity to retain functional macroalgal chloroplasts inside their cells. This endosymbiotic association is nutritionally relevant for these organisms and represents an interesting research issue for biotechnological applications. The Caribbean species Elysia crispata can integrate chloroplasts from different macroalgal species. The lipidome of chloroplasts includes lipid classes unique to these photosynthetic organelles. Specialized lipids, such as the glycolipids MGDG, DGDG, and SQDG, are essential for maintaining the integrity of both the thylakoid membranes and the overall chloroplast membrane structure. Additionally, lipids are a diverse group of biomolecules playing essential roles at nutritional and physiological levels. A combined approach using LC-HR-MS and MS/MS was employed to determine the polar lipid profile of the photosynthetic sea slug E. crispata from two habitats in the north-western tropical Atlantic (Sistema Arrecifal Veracruzano and Mahahual) and two different feeding conditions (fed and after 1 week of starvation). Significant differences were identified in the abundance of structural and signalling phospholipids (PC, PI, PG, PS, CL) suggesting different nutritional states between populations. The composition of glycolipids demonstrated a clear separation by habitat, but not by feeding conditions. The lower abundance of glycolipids in the Mahahual samples suggests a lower density of chloroplasts in their tissues compared to Veracruz individuals. These results corroborate that 1 week of starvation is insufficient to initiate the degradation of plastid membranes. This study confirms the advantages of using lipidomics as a tool to enhance our knowledge of the ecology of marine invertebrates.

Supplementary information: The online version contains supplementary material available at 10.1007/s42995-025-00281-1.

Keywords: Kleptoplasty; Lipidomics; Marine invertebrates; Marine lipids; Photosynthetic animals; Polar lipids.

Fig. 1

Coral reefs where Elysia crispata specimens were sampled in southern Gulf of Mexico (Veracruz) and the Mexican Caribbean (Mahahual) and specimens from each sampling area

Fig. 2

Chord diagrams showing the flows of normalized extracted-ion chromatogram (XIC) areas of A total lipids, and the main classes of B phospholipids (PL), C glycolipids (GL), D sphingolipids (SL) and E betaine lipids (BL) identified in Elysia crispata collected in two different habitats, Veracruz (Vera) and Mahahual (Maha) and under two different feeding conditions, fed and 1 week of starvation. XIC displays the signal intensity of mass-to-charge (m/z) values which were normalized by the XIC area of the corresponding internal standard

Fig. 3

Polar lipidome profile. A Phospholipid, B glycolipid, C sphingolipid and D betaine lipids classes identified in Elysia crispata collected in two different habitats, Veracruz (Vera) and Mahahual (Maha) and under two different feeding conditions, fed and 1 week of starvation. Data represent sum of normalized extracted-ion chromatogram (XIC) areas for each lipid class

Fig. 4

Principal component analysis (PCA) of log-transformed normalized extracted-ion chromatogram (XIC) areas of A total lipid species, B phospholipids, C glycolipids, D sphingolipids and E betaine lipids identified in Elysia crispata collected in two different habitats, Veracruz (Vera) and Mahahual (Maha) and under two different feeding conditions, fed and 1 week of starvation

Fig. 5

Heatmap/clustering analysis showing the top 50 most significant lipid species in A total lipid species, B phospholipids and C glycolipids discriminating Elysia crispata collected in two different habitats, Veracruz (Vera) and Mahahual (Maha) and under two different feeding conditions, fed and 1 week of starvation

Fig. 6

A Principal component analysis (PCA) of log-transformed normalized extracted-ion chromatogram (XIC) areas and B heatmap/clustering analysis (PCA) showing the top 50 most significant lipid species discriminating Elysia crispata sampled in two different habitats Veracruz (Vera) and Mahahual (Maha) under fed conditions. C PCA of log-transformed XIC areas and D heatmap/clustering analysis showing the top 50 most significant lipid species discriminating E. crispata sampled in two different habitats Veracruz (Vera) and Mahahual (Maha) and starved for a week

Fig. 7

Molecular species that showed significant differences in the comparison between fed versus starved Elysia crispata sampled in two different habitats, Veracruz (fed vs. starved) and Mahahual (fed vs. starved), (Student’s t test, p < 0.05, with FDR correction). The lipid species that significantly incremented under starved conditions were marked in bold