Thylakoid membranes are specialized membranes predominantly composed of uncommon galacto-and sulfolipids, having distinct roles in photosynthesis. Large acyl chain variety and richness in polyunsaturated fatty acid (PUFA) content of thylakoid lipids further add to the compositional complexity. The function of these membrane systems is intimately dependent on the fluidity of its lipid matrix, which is strongly modulated by the lipid composition and temperature. The present work, employing extensive atomistic simulations, provides the first atomistic view of the phase transition and domain coexistence in a model membrane composed of thylakoid lipids of a commercially important red alga Gracilaria corticata between 10 and 40 °C. The growth and photosynthetic activity of marine algae are greatly influenced by the seawater temperature. So far, little is known about the molecular organization of lipids in thylakoid membranes, in particular their adaptive arrangements under temperature stress. Our simulations show that the algal thylakoid membrane undergoes a transition from a gel-like phase at a low temperature, 10−15 °C, to a homogeneous liquid-crystalline phase at a high temperature, 40 °C. Clear evidence of spontaneous phase separation into coexisting nanoscale domains is detected at intermediate temperatures nearing the optimal growth temperature range. Particularly, at 25−30 °C, we identified the formation of a stable ripple phase, where the gel-like domains rich in saturated and nearly hexagonally packed lipids were separated from fluid-like domains enriched in lipids containing PUFA chains. The phase separation is driven by the spontaneous and preferential segregation of lipids into differentially ordered domains, mainly depending on the acyl chain types. Cholesterol impairs the phase transition and the emergence of domains and induces a fairly uniform liquid-ordered phase in the membrane over the temperatures studied. This work improves the understanding of the properties and reorganization of lipids in the thylakoid membrane in response to temperature variation.

Marine algae are diverse photosynthetic organisms, profoundly rich in bioactive compounds. Temperature is a major factor in algal cultivation and biomass production. At the cellular level, the change of temperature is reflected in oscillating algal lipid/fatty acid profile and inhibition of photosynthetic activities. The function of thylakoid membrane system is intimately dependent on its lipid matrix, however the molecular organization of these lipid membranes and particularly their adaptive arrangements under temperature stress remain largely unexplored. The present work employing extensive atomistic simulations provides the first atomistic view of the phase transition and domain coexistence in model membrane composed of thylakoid lipids of a marine alga, between 10-40 °C. The model membrane undergoes a transition from a gel-like phase at 10-15 °C to a homogeneous liquid-disordered phase at 40 °C. Clear evidences of spontaneous phase separation into coexisting nanoscale domains are detected at intermediate temperatures. Particularly at 25-30 °C, we identified the formation of a stable rippled phase, where the gel-like domains rich in saturated and nearly hexagonally packed lipids separated from fluid-like domains enriched in lipids containing polyunsaturated chains. Cholesterol impairs the phase transition and the emergence of domains, and induces a fairly uniform liquid-ordered phase in the membrane over the temperatures studied. The results have implications in understanding the role of lipids in temperature adaptation in algal.