Organization and Assembly of Light-Harvesting Complexes in the Purple Bacterial Membrane

Abstract

Recent in situ surface images of the intracytoplasmic membrane (ICM) of purple photosynthetic bacteria obtained at submolecular resolution by atomic force microscopy (AFM), have revealed multiple, species-dependent patterns of supramolecular organizations for their light-harvesting (LH) antennas, suggested earlier from spectroscopic studies. These have varied from highly ordered linear arrays of dimeric reaction center-light-harvesting 1-PufX (RC-LH1-PufX) core complexes in Rhodobacter (Rba.) sphaeroides, with the peripheral LH2 antenna either interspersed between them or arranged in larger clusters, to a less orderly arrangement found in several other purple bacteria, in which randomly organized, monomeric RC-LH1-enriched domains co-exist with large, paracrystalline hexagonally packed LH2 domains. In addition, regions with apparently crystalline core complexes were observed in Rhodopseudomonas (Rps.) palustris, along with a protein-free lipid bilayer. Likely bases for the absence of the ATP synthase and cytochrome bc 1 complex from the AFM topographs are discussed, including the possibility that they localize at the poles of ICM vesicles either out of view of flat regions imaged by AFM, or are removed during membrane preparation. We also discuss how the observed arrangements of LH2 and core complexes may specifically control quinol escape from the RC, emphasizing the importance of short-range diffusion within the disordered regions of the membrane in promoting the passage of quinone, and how this process may be augmented by quinone exclusion from large, ordered fields of the LH2 antenna. Possible forces that drive in vitro autoassembly of LH complexes are assessed along with the roles that complex-specific and general membrane assembly factors may play in driving the assembly and organization of photosynthetic units within the cell. Finally, we address likely perspectives for further studies on the organization and assembly of bacterial antenna complexes over the next decade.