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

The capacity to retain long-term functional algal chloroplasts within animal cells is a singular trait of certain Sacoglossa sea slugs. The sequestered chloroplasts (kleptoplasts) confer photosynthetic capacity to the host. Photosynthetic organisms possess distinctive lipid classes that are essential for chloroplast membrane integrity and photosynthetic function. This study investigated how chloroplast lipidomes from two macroalgae (Acetabularia acetabulum and Bryopsis sp.) are remodelled following sequestration by the photosynthetic sea slugs Elysia crispata, Elysia viridis, and Elysia timida. Pigments were analysed by HPLC, and lipidomic profiling of chloroplasts, focusing on glycolipids, betaine lipids and phytosterols, was conducted using C18-LC-MS/MS. Kleptoplasts preserved an intact algal pigment profile across hosts. Glycolipid signatures in sea slug tissues closely resembled those of their algal donors, although shifts in relative abundances suggested post-sequestration remodelling of plastidial membranes, with potential consequences on membrane curvature, stability and kleptoplast morphology. In contrast, betaine lipid composition diverged markedly between sea slugs and algal donors, with a set of dominant betaine species shared among 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 retain strong algal identity while undergoing selective modifications within the animal host. Host-associated modifications likely tune membrane architecture to support long-term stability and photosynthetic functionality within the hosts’ cellular environment, facilitating the integration and performance of sea slug kleptoplasts.