Lipidomic remodelling during photosynthesis decline in kleptoplastidic sea slugs: glycolipids and sterols as candidate biomarkers of kleptoplasty.

Abstract

Some sacoglossan sea slugs can acquire and retain chloroplasts from their algal prey, enabling them to use light energy to synthesize organic compounds, a process known as kleptoplasty. The lifespan of these stolen chloroplasts (kleptoplasts) is limited, and sea slugs must feed regularly to maintain high levels of photosynthetic activity. Lipids are essential molecules of cell membranes, energy storage, and signalling pathways, and may be involved in chloroplast retention and functionality within the host animal cells. Advanced lipidomics techniques (C18-LC-HR-MS/MS) were used to investigate changes in the lipid profile associated with decreased photosynthetic activity in the kleptoplastidic sea slugs Elysia viridis and Elysia crispata under starvation conditions, after feeding on Codium tomentosum and Bryopsis sp. In both sea slugs, glycolipids, unique to chloroplast membranes, decreased markedly in the absence of algal food sources. The rate of glycolipid decline depended on both the sea slug species and the chloroplast donor, indicating species- and diet-dependent differences in the timing and pattern of kleptoplast degradation. Sterols increased in sea slugs that experienced reduced photosynthetic efficiency, potentially reflecting lipid recycling and/or stress-associated lipid metabolism. These findings reveal lipidomic changes associated with starvation-induced photosynthetic decline in kleptoplastidic sea slugs and position glycolipids and sterols as candidate biomarkers for assessing kleptoplast integrity and functional kleptoplasty.

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