Structures of a phycobilisome in light-harvesting and photoprotected states

Abstract

The phycobilisome is an elaborate antenna that is responsible for light-harvesting in cyanobacteria and red-algae. This large macromolecular complex captures incident sunlight and transfers the energy via a network of pigment molecules called bilins to the photosynthetic reaction centers. The phycobilisome of the model organism Synechocystis PCC 6803 consists of a core to which six rods are attached but its detailed molecular architecture and regulation in response to environmental conditions is not well understood. Here we present cryo-electron microscopy structures of the 6.2 MDa phycobilisome from Synechocystis PCC 6803 resolved at 2.1 Å (rods) to 2.7 Å (core), revealing three distinct conformations, two previously unknown. We found that two of the rods are mobile and can switch conformation within the complex, revealing a layer of regulation not described previously. In addition, we found a novel linker protein in the structure, that may represent a long-sought subunit that tethers the phycobilisome to the thylakoid membrane. Finally, we show how excitation energy is transferred within the phycobilisome and correlate our structures with known spectroscopic properties. Together, our results provide detailed insights into the biophysical underpinnings of cyanobacterial light harvesting and lay the foundation for bioengineering of future phycobilisome variants and artificial light harvesting systems.

Stages of OCP-FRP Interactions in the Regulation of Photoprotection in Cyanobacteria, Part 1: Time-Resolved Spectroscopy

“…Recent structural data by Dominguez-Martin et al indicates that the dimer of the red OCP R form interacts with the core of the phycobilisome. 43 The presence of dimeric OCP R was also observed in solution in previous SANS 44 and TR-SAXS experiments. 45 As shown by the small-angle X-ray and neutron scattering experiments presented in the accompanying paper, two FRP dimers can interact with the functional dimeric red OCP R complex simultaneously, but the FRP structure undergoes conformational changes.…”

“…We believe that, in the cyanobacterial cell, the dimeric OCP R form can play a functional role as its concentration is kept high by the low rate of its relaxation. Recent structural data by Dominguez-Martin et al indicates that the dimer of the red OCP R form interacts with the core of the phycobilisome . The presence of dimeric OCP R was also observed in solution in previous SANS and TR-SAXS experiments .…”

Large-scale FRET simulations reveal the control parameters of phycobilisome light-harvesting complexes

“…This effect is present in a simulation performed on the recently published Synechocystis sp. PCC6803 PBS structure [ 25 ]. Two neighbouring rods were selected, and the two hexamers proximal to the core from each rod were used to create a model for simulation by aligning template dipoles to the phycocyanin chromophores ( figure 8 ).…”

“…These structures are massive, containing 14 rods and 1598 light-absorbing chromophore molecules. More recently, the Kerfeld lab resolved the structure of a cyanobacterial PBS containing four orange carotenoid proteins (OCP) [ 25 ]. These structures provide a good deal of here-to-unknown structural information and a basis for understanding changes in PBS efficiency, through energy transfer simulations [ 25 ].…”

“…More recently, the Kerfeld lab resolved the structure of a cyanobacterial PBS containing four orange carotenoid proteins (OCP) [ 25 ]. These structures provide a good deal of here-to-unknown structural information and a basis for understanding changes in PBS efficiency, through energy transfer simulations [ 25 ]. However, these simulations did not calculate dynamic quantum effects.…”