Abstract
The role of non-bilayer lipids and non-lamellar lipid phases in biological membranes is an enigmatic problem of membrane biology. Non-bilayer lipids are present in large amounts in all membranes; in energy-converting membranes they constitute about half of their total lipid content—yet their functional state is a bilayer. In vitro experiments revealed that the functioning of the water-soluble violaxanthin de-epoxidase (VDE) enzyme of plant thylakoids requires the presence of a non-bilayer lipid phase. 31P-NMR spectroscopy has provided evidence on lipid polymorphism in functional thylakoid membranes. Here we reveal reversible pH- and temperature-dependent changes of the lipid-phase behaviour, particularly the flexibility of isotropic non-lamellar phases, of isolated spinach thylakoids. These reorganizations are accompanied by changes in the permeability and thermodynamic parameters of the membranes and appear to control the activity of VDE and the photoprotective mechanism of non-photochemical quenching of chlorophyll-a fluorescence. The data demonstrate, for the first time in native membranes, the modulation of the activity of a water-soluble enzyme by a non-bilayer lipid phase.
Highlights
The role of non-bilayer lipids and non-lamellar lipid phases in biological membranes is an enigmatic problem of membrane biology
Spectroscopy to identify different lipid phases in artificial and native systems has been thoroughly documented (e.g.41, 42). This technique has revealed the polymorphic phase behaviour of isolated plant thylakoid membranes and uncovered that non-lamellar lipid phases play an active role in the structural dynamics of thylakoid membranes[27, 29]
We revealed characteristic low-pH and thermally-induced reversible enhancements and peak shifts of the isotropic phases in isolated spinach thylakoid membranes
Summary
The role of non-bilayer lipids and non-lamellar lipid phases in biological membranes is an enigmatic problem of membrane biology. We reveal reversible pH- and temperature-dependent changes of the lipid-phase behaviour, the flexibility of isotropic non-lamellar phases, of isolated spinach thylakoids These reorganizations are accompanied by changes in the permeability and thermodynamic parameters of the membranes and appear to control the activity of VDE and the photoprotective mechanism of non-photochemical quenching of chlorophyll-a fluorescence. The primary function of biological membranes is to allow compartmentalization of cells and cellular organelles and, in general, the separation of two aqueous phases with different compositions. The functioning of these membranes, at the basic level, depends on the organization of their lipid molecules into bilayer s tructures[1,2,3]. The primary charge separation in the photochemical reaction centers and the consecutive vectorial electron and proton transport processes generate a transmembrane ΔpH (acidification of the lumen by 2–3 pH units) and an electric potential gradient (ΔΨ, of approximately 1 05 V cm−1), components of the proton-motive force
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