Structure and quenching of a bundle-shaped phycobilisome

Cyanobacteria use soluble antenna megacomplexes, phycobilisomes (PBSs), to maximize light-harvesting efficiency and small photoswitchable orange carotenoid proteins (OCPs) to down-regulate PBSs in high light. Among known PBS morphologies, the one from the basal cyanobacterial genus <i>Gloeobacter</i> still lacks detailed structural characterization. Here, we reconstructed a cryo-electron microscopy structure of the >10-megadalton <i>Gloeobacter violaceus</i> PBS, with diverging, conformationally mobile bundles of rods composed of stacked phycoerythrin and phycocyanin hexamers, stemming from a pentacylindrical allophycocyanin core belted by auxiliary phycocyanin hexamers. We show how two <i>Gloeobacter</i>-specific multidomain linker proteins, Glr1262 and Glr2806, maintain this bundle-shaped architecture and reveal its differential regulation via nonphotochemical quenching by two OCP types of <i>G. violaceus</i> that recognize separate binding sites within the allophycocyanin core, including lateral cylinders absent in tricylindrical cores.