Phase Transition and Phase Separation in Realistic Thylakoid Lipid Membrane of Marine Algae in All-Atom Simulations

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.