Origin of Cyanobacteria thylakoids via a non-vesicular glycolipid phase transition and impact on the Great Oxygenation Event.

Appearance of oxygenic photosynthesis in Cyanobacteria is a major event in the evolution of Life. It had an irreversible impact on our planet, promoting the Great Oxygenation Event (GOE), ~2.4 b.y.a. Ancient Cyanobacteria predating the GOE were Gloeobacter-type cells, having no thylakoids. They hosted photosystems in their cytoplasmic membrane. The driver of the GOE was proposed to be the transition from unicellular to filamentous Cyanobacteria. However, the appearance of thylakoids expanded the photosynthetic surface by multiple logs: this multiplier effect would be more coherent with an impact on the atmosphere. Primitive thylakoids self-organize as concentric parietal uninterrupted multilayers. The quest for their origin resists vesicular-based scenarios. This review reports studies supporting that Hexagonal II-forming gluco- and galactolipids at the periphery of the cytosolic membrane could be turned within nanoseconds and without any external source of energy into membrane multilayers. Comparison of lipid biosynthetic pathways further shows that ancient Cyanobacteria contained only one anionic Lamellar-forming lipid, phosphatidylglycerol. Acquisition of sulfoquinovosyldiacylglycerol biosynthesis correlates with thylakoid emergence, possibly enabling a sufficient provision of anionic lipids to trigger an Hexagonal II-to-Lamellar phase transition. With this non-vesicular lipid-phase transition, a framework is also available to reexamine the role of companion proteins in thylakoid biogenesis processes.