Abstract
Xanthophylls (polar carotenoids) play diverse biological roles, among which are modulation of the physical properties of lipid membranes and protection of biomembranes against oxidative damage. Molecular mechanisms underlying these functions are intimately related to the localization and orientation of xanthophyll molecules in lipid membranes. In the present work, we address the problem of localization and orientation of two xanthophylls present in the photosynthetic apparatus of plants and in the retina of the human eye, zeaxanthin and lutein, in a single lipid bilayer membrane formed with dimyristoylphosphatidylcholine. By using fluorescence microscopic analysis and Raman imaging of giant unilamellar vesicles, as well as molecular dynamics simulations, we show that lutein and zeaxanthin adopt a very similar transmembrane orientation within a lipid membrane. In experimental and computational approach, the average tilt angle of xanthophylls relative to the membrane normal is independently found to be ~40 deg, and results from hydrophobic mismatch between the membrane thickness and the distance between the terminal hydroxyl groups of the xanthophylls. Consequences of such a localization and orientation for biological activity of xanthophylls are discussed.
Highlights
Carotenoids, including polar xanthophylls, are ubiquitous in nature and play numerous physiological roles, among which are modulation of the physical properties of lipid membranes and protection against oxidative damage of membrane lipids[1,2,3]
High fluorescence anisotropy levels, manifested by red color according to the color coded scale, in the left-hand and right-hand sectors of the liposomes, both in the case of Lut and Zea, indicates roughly vertical orientation of both xanthophylls in the membrane
The orientation angles of Zea (42.7 ± 0.9) and Lut (41.8 ± 1.4), determined in a single lipid bilayer, are very close to each other
Summary
Carotenoids, including polar xanthophylls, are ubiquitous in nature and play numerous physiological roles, among which are modulation of the physical properties of lipid membranes and protection against oxidative damage of membrane lipids[1,2,3]. Localization, organization and orientation of xanthophyll molecules within the lipid bilayers (see the model presented in Fig. 1) are tightly associated with molecular mechanisms responsible for physiological activity of carotenoids in biomembranes and such problems were frequently addressed in the past, in advanced studies[4,5,6,7]. Involvement of Zea in the reactions of the xanthophyll cycle makes this pigment at least temporarily present and functional directly in the lipid phase of the thylakoid membranes[16,17,18] Owing to this fact, localization and orientation of Zea in lipid bilayers is a problem interesting and important from the standpoint of photosynthesis research
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