Abstract
Sacoglossan sea slugs, also known as crawling leaves due to their photosynthetic activity, are highly selective feeders that incorporate chloroplasts from specific macroalgae. These “stolen” plastids - kleptoplasts - are kept functional inside animal cells and likely provide an alternative source of energy to their host. The mechanisms supporting the retention and functionality of kleptoplasts remain unknown. A lipidomic mass spectrometry-based analysis was performed to study kleptoplasty of the sacoglossan sea slug Elysia viridis fed with Codium tomentosum. Total lipid extract of both organisms was fractionated. The fraction rich in glycolipids, exclusive lipids from chloroplasts, and the fraction rich in betaine lipids, characteristic of algae, were analysed using hydrophilic interaction liquid chromatography-mass spectrometry (HILIC-LC-MS). This approach allowed the identification of 81 molecular species, namely galactolipids (8 in both organisms), sulfolipids (17 in C. tomentosum and 13 in E. viridis) and betaine lipids (51 in C. tomentosum and 41 in E. viridis). These lipid classes presented similar lipidomic profiles in C. tomentosum and E. viridis, indicating that the necessary mechanisms to perform photosynthesis are preserved during the process of endosymbiosis. The present study shows that there are no major shifts in the lipidome of C. tomentosum chloroplasts sequestered by E. viridis.
Highlights
Sacoglossan sea slugs have been popularly termed as crawling leaves[1] due to their singular relationship with their food
HILIC-LC-MS and MS/MS allowed the identification of glycolipids and betaine lipids in the lipid extracts obtained from the marine species C. tomentosum and E. viridis
Glycolipids were identified in fraction 3 for both C. tomentosum and E. viridis, distributed between galactolipid (MGDG and digalactosyl diacylglycerol (DGDG)) and sulfolipid classes
Summary
Sacoglossan sea slugs have been popularly termed as crawling leaves[1] due to their singular relationship with their food. While kleptoplasty is a general phenomenon in protists[13, 14], to date, sacoglossans are the only metazoans known to maintain this type of association[15] This mechanism of endosymbiosis could have some similar features to the interaction between eukaryotic cells and endosymbiotic cyanobacteria, which gave rise to chloroplast-containing eukaryotes[12]. Lipidomic analyses applied to marine samples can provide information at the molecular level, being successfully used to explain biological and molecular processes[24,25,26] In this sense, we selected the ecological model E. viridis (Montagu, 1804) and Codium tomentosum (Stackhouse, 1797) to investigate the association of functional macroalgal chloroplasts inside animal cells, by using lipidomic tools. E. viridis displays a relatively long-term retention of kleptoplasts[3, 4], which allows researchers to perform experiments on individuals that already display well established functional kleptoplasts inside their animal cells
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