Preservation and remodelling of chloroplast lipids in photosynthetic sea slug host cells

Abstract

The capacity to retain long-term functional algal chloroplasts within animal cells is a singular trait of some Sacoglossa sea slugs. The stolen chloroplasts (kleptoplasts) confer photosynthetic capacity to the host. This study investigated how chloroplast lipidomes from two macroalgae (Acetabularia acetabulum and Bryopsis sp.) are modified after sequestration by the photosynthetic sea slugs Elysia crispata, Elysia viridis, and Elysia timida. Pigments were analysed by HPLC, and lipidomic profiling of chloroplasts (glycolipids, betaine lipids, phytosterols) was conducted using C18-LC-MS/MS. Kleptoplasts retain intact algal pigment profile. Glycolipid signatures in sea slug tissues closely resembled those of their algal donors, although shifts in relative abundances suggest remodelling of plastidial membranes, potentially affecting kleptoplast morphology, particularly membrane curvature and stability. In contrast, betaine lipid composition differed markedly between sea slugs and algal donors, with major betaine species common to all sea slugs. Phytosterol composition was better preserved in sea slugs feeding on Bryopsis sp. than on A. acetabulum. This study demonstrated that kleptoplast lipidomes maintain a strong algal identity but undergo selective modifications within the animal host. This remodelling likely optimizes membrane architecture to support long-term stability and photosynthetic functionality within the hosts cellular environment, facilitating the integration and performance of sea slug kleptoplasts. HighlightThe lipid profiles of photosynthetic sea slugs resemble the algal donors chloroplasts. However, alterations in glycolipid composition suggest that the molecular architecture of kleptoplasts is modulated by the host cells.