Structural and functional roles of non-bilayer lipid phases of chloroplast thylakoid membranes and mitochondrial inner membranes

• Published in: Progress in lipid research 2022-04, Vol.86, p.101163-101163, Article 101163
• Main Authors: Garab, Győző, Yaguzhinsky, Lev S., Dlouhý, Ondřej, Nesterov, Semen V., Špunda, Vladimír, Gasanoff, Edward S.
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate; Animals; ATP synthesis; Dynamic exchange between lipid phases; Fusion and fission of membranes; Inner mitochondrial membranes; Lipid Bilayers; Lipids - chemistry; Mammals; Mitochondrial Membranes; Non-bilayer lipids; Thylakoid membranes; Thylakoids - chemistry; Water
• ISSN: 0163-7827; 1873-2194
• DOI: 10.1016/j.plipres.2022.101163

The ‘standard’ fluid-mosaic membrane model can provide a framework for the operation of the photosynthetic and respiratory electron transport systems, the generation of the proton motive force (pmf) and its utilization for ATP synthesis according to the chemiosmotic theory. However, this model, with the bilayer organization of all lipid molecules, assigns no function to non-bilayer lipids – while in recent years it became clear that the two fundamental energy transducing membranes of the biosphere, chloroplast thylakoid membranes (TMs) and inner mitochondrial membranes (IMMs), contain large amounts of non-bilayer (non-lamellar) lipid phases. In this review, we summarize our understanding on the role of non-lamellar phases in TMs and IMMs: (i) We propose that for these membrane vesicles the dynamic exchange model (DEM) provides a more suitable framework than the ‘standard’ model; DEM complements the ‘standard’ model by assuming the co-existence of bilayer and non-bilayer phases and their interactions, which contribute to the structural dynamics of the membrane systems and safe-guard the membranes’ high protein:lipid ratios. (ii) Non-bilayer phases play pivotal roles in membrane fusion and intermembrane lipid exchanges – essential processes in the self-assembly of these highly folded intricate membranes. (iii) The photoprotective, lipocalin-like lumenal enzyme, violaxanthin de-epoxidase, in its active state requires the presence of non-bilayer lipid phase. (iv) Cardiotoxins, water-soluble polypeptides, induce non-bilayer phases in mitochondria. (v) ATP synthesis, in mammalian heart IMMs, is positively correlated with the amount of non-bilayer packed lipids with restricted mobility. (vi) The hypothesized sub-compartments, due to non-lamellar phases, are proposed to enhance the utilization of pmf and might contribute to the recently documented functional independence of individual cristae within the same mitochondrion. Further research is needed to identify and characterize the structural entities associated with the observed non-bilayer phases; and albeit fundamental questions remain to be elucidated, non-lamellar lipid phases should be considered on a par with the bilayer phase, with which they co-exist in functional TMs and IMMs. •Functional thylakoid and mitochondrial membranes display marked lipid polymorphisms.•Fusion, dynamics and plasticity of membranes depend largely on non-bilayer phases.•Non-bilayer propensity of lipids safe-guards the membranes’ hi