Probing the biogenesis pathway and dynamics of thylakoid membranes_C4PR_LIV

Thylakoid membranes are the specialized internal membrane system produced in plants, algae, and cyanobacteria to convert sunlight to chemical energy via oxygenic photosynthesis. Cyanobacterial thylakoid membranes harbor the protein complexes and electron transport molecules that are necessary for photosynthetic light reactions and respiratory electron flow. The thylakoid membranes sit between the plasma membrane and the central cytoplasm, leading to intricate cellular compartmentalization. How thylakoid membranes are generated to form the functional network and how protein complexes are recruited into thylakoids remain elusive. Here, we developed a method to modulate thylakoid biogenesis in the model cyanobacterium Synechococcus elongatus PCC7942 and probed the spatial-temporal stepwise biogenesis process of cyanobacterial thylakoid membranes, using electron microscopy, in situ cryo-electron tomography, confocal microscopy, mass spectroscopy, and biochemical approaches. Our results revealed that the plasma membrane and regularly-arranged concentric thylakoid layers have no physical connections. The newly synthesized thylakoid membrane fragments commerce between the plasma membrane and pre-existing thylakoids, where the initial biogenesis of Photosystem II occurs. Photosystem I monomers appear in thylakoid membranes earlier than other photosystem assemblies. Redistribution of photosynthetic protein complexes during thylakoid biogenesis ensures establishment of the spatial organization of the functional thylakoid membrane network. This study provides insights into the molecular processes of the photosynthetic machinery biosynthesis and organization.