Decoupling of plastid and endomembrane homeoviscous response to low temperature and darkness in Phaeodactylum tricornutum.

backgroundGlycerolipids, essential for biological membranes, have diverse structures based on their fatty acids and polar head groups. In photosynthetic organisms, fatty acids are synthesized in plastids as saturated acyl chains that can be desaturated and/or incorporated into lipids like mono- and digalactosyldiacylglycerol, sulfoquinovosyldiacylglycerol, and phosphatidylglycerol. Environmental changes, such as temperature drops, reduce membrane fluidity, prompting cells to respond by remodeling their lipids; including an increase in long-chain polyunsaturated fatty acids to maintain membrane function.. Diatoms, key marine phytoplankton, thrive in fluctuating conditions and adapt through mechanisms like lipid remodeling during temperature drops or darkness. Their ecological relevance in marine ecosystems may stem from the diverse functional repertoire encoded by their chimeric genomes, an outcome of serial endosymbiotic events, which have likely contributed to their evolutionary success. To study its lipidomic response, the diatom Phaeodactylum tricornutum was exposed to 10 °C, darkness, or both, revealing adaptive changes compared to control conditions at 20 °C with 12:12 light:dark photoperiods.

resultsExposure to 10 °C and darkness in P. tricornutum induced a significant variation in lipid and fatty acid profiles. Phosphatidylcholine and phosphatidylethanolamine increased, while mono- and digalactosyldiacylglycerol decreased. Triacylglycerols were undetectable in darkness, aligning with their synthesis through neosynthesis rather than lipid remodeling. Fatty acid unsaturation increased under cold in plastidial Lipids, while in phosphatidylglycerol it was reduced at 10 °C but increased in darkness. Cold significantly elevated unsaturated phosphatidylcholine and phosphatidylethanolamine species. Light exposure was crucial for low-temperature adaptation in plastidial lipids, as darkness inhibited specific remodeling, suggesting light-dependent regulatory mechanisms for membrane fluidity and functionality under cold stress.

conclusionsOur study reveals significant shifts in plastidial lipid species and unsaturation levels in P. tricornutum under low temperatures and extended darkness, showing lipid remodeling's importance in maintaining membrane fluidity and protecting photosynthetic systems. Light activates plastidial Lipid remodeling, notably the 16:3-to-16:4 switch, suggesting a light-dependent regulatory mechanism. Endomembrane lipid remodeling appears less light-dependent. These findings enhance understanding of diatom adaptation to environmental fluctuations, crucial for their resilience in diverse marine environments. Future research should explore molecular pathways and species-specific strategies in other diatom species, especially polar taxa.