Light-induced structural adaptation of the bundle-shaped phycobilisome from thylakoid-lacking cyanobacterium...

Gloeobacter diverged from other lineages early in cyanobacterial evolution, preferentially growing under low light intensity conditions. Among cyanobacteria, G. violaceus exhibits unique features, including lack of a thylakoid membrane and bundle-shaped antenna phycobilisomes (PBSs), densely packed and well-organized on the plasma membrane. However, without high-resolution structures, it has remained unclear how G. violaceus PBSs assemble into a bundle-shaped configuration. Here we solve the cryo-EM structures of PBSs from G. violaceus cells cultured under low (Sr-PBS) or moderate (Lr-PBS) light intensity. These structures reveal two unique linker proteins, L_RC^91kDa and L_RC^81kDa, that play a key role in the PBS architecture. Analysis of the bilin arrangement indicates that the bundle-shaped structure allows efficient energy transfer among rods. Moreover, comparison between Lr-PBS and Sr-PBS uncovers a distinct mode of adaption to increased light intensity wherein the ApcA₂-ApcB₃-ApcD layer can be blocked from binding to the core by altering structural elements exclusively found in the G. violaceus L_CM. This study illustrates previously unrecognized mechanisms of assembly and adaptation to varying light intensity in the bundle-shaped PBS of G. violaceus.