Temperature-Induced Lipid Remodeling Underpins Thermal Resilience in Marine Macroalgae via Homeoviscous Membrane Adaptation: Bridging Experiments and Atomistic Simulations

Marine macroalgae are vital primary
producers of coastal
ecosystems
and natural sources of industrially-important bioactive compounds.
Temperature governs their productivity, while ocean warming and extreme
marine heatwaves amid climate change threaten their survival. Integrating
experiments and molecular dynamics (MD) simulations, this study for
the first time unravels how lipid remodeling contributes to the thermal
acclimation mechanism of Kappaphycus alvareziia carrageenan-producing marine macroalga widely cultivated
in tropics and subtropics. We have elucidated the adaptive rearrangement
in fatty acid compositions across temperatures and its consequence
on the stability of thylakoid membranes, the primary photosynthesis
sites, in tight correlation with macroalgal physiological traits.
Upon exposure to 20–34 °C, K. alvarezii exhibits steady growth and photosynthetic performances but rapidly
loses biomass and pigments at 41 °C. Consequently, its fatty
acid composition shows strong temperature responsiveness, clearly
transiting from the highest polyunsaturated fatty acids (PUFAs) (∼52%
of TFA) at lowest to nearly complete saturation (∼97%) at highest
temperature. Within the acclimation range of 20–34 °C,
the unsaturation index gradually and linearly decreases with temperature.
Atomistic simulations reveal that such lipidomic restructuring efficiently
enforces identical fluidity and lipid packing in thylakoid membranes
despite altered growth temperatures, providing the first compelling
evidence of homeoviscous adaptation in marine macroalgae. However,
at 41 °C, the drastic loss of 20:4(n-6) and
20:5(n-3) PUFAs leads to membrane rigidification
and gel phase formation, coinciding with halted growth and photosynthesis.
We propose that sustaining adequate PUFA levels may restore collective
membrane properties at elevated temperatures. Our study suggests cellular
membranes as a critical interface in macroalgal thermotolerance, whose
homeostatic tuning ensures the cellular functionality across shifting
thermal regimes.