Ma, J.; You, X.; Sun, S.; Sui, S.-F.

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 solved the cryo-EM structures of PBSs from G. violaceus cells cultured under low (Sr-PBS) or moderate (Lr-PBS) light intensity. These structures revealed two unique linker proteins, LRC91kDa and LRC81kDa, that play a key role in the PBS architecture. Analysis of the bilin arrangement indicated that the bundle-shaped structure allows efficient energy transfer among rods. Moreover, comparison between Lr-PBS and Sr-PBS uncovered 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 LCM. This study illustrates previously unrecognized mechanisms of assembly and adaptation to varying light intensity in the bundle-shaped PBS of G. violaceus.