Structural diversity and modularity of photosynthetic RC-LH1 complexes.

Bacterial photosynthesis is essential for sustaining life on Earth as it aids in carbon assimilation, atmospheric composition, and ecosystem maintenance. Many bacteria utilize anoxygenic photosynthesis to convert sunlight into chemical energy while producing organic matter. The core machinery of anoxygenic photosynthesis performed by purple photosynthetic bacteria and Chloroflexales is the reaction center-light-harvesting 1 (RC-LH1) pigment-protein supercomplex. In this review, we discuss recent structural studies of RC-LH1 core complexes based on the advancement in structural biology techniques. These studies have provided fundamental insights into the assembly mechanisms, structural variations, and modularity of RC-LH1 complexes across different bacterial species, highlighting their functional adaptability. Understanding the natural architectures of RC-LH1 complexes will facilitate the design and engineering of artificial photosynthetic systems, which can enhance photosynthetic efficiency and potentially find applications in sustainable energy production and carbon capture.

Cryo-EM structure of a monomeric RC-LH1-PufX supercomplex with high-carotenoid content from Rhodobacter capsulatus.

In purple photosynthetic bacteria, the photochemical reaction center (RC) and light-harvesting complex 1 (LH1) assemble to form monomeric or dimeric RC-LH1 membrane complexes, essential for bacterial photosynthesis. Here, we report a 2.59-Å resolution cryoelectron microscopy (cryo-EM) structure of the RC-LH1 supercomplex from Rhodobacter capsulatus. We show that Rba. capsulatus RC-LH1 complexes are exclusively monomers in which the RC is surrounded by a 15-subunit LH1 ring. Incorporation of a transmembrane polypeptide PufX leads to a large opening within the LH1 ring. Each LH1 subunit associates two carotenoids and two bacteriochlorophylls, which is similar to Rba. sphaeroides RC-LH1 but more than one carotenoid per LH1 in Rba. veldkampii RC-LH1 monomer. Collectively, the unique Rba. capsulatus RC-LH1-PufX represents an intermediate structure between Rba. sphaeroides and Rba. veldkampii RC-LH1-PufX. Comparison of PufX from the three Rhodobacter species indicates the important residues involved in dimerization of RC-LH1.

Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC-LH1 supercomplex.

The reaction center (RC) and light-harvesting complex 1 (LH1) form a RC-LH1 core supercomplex that is vital for the primary reactions of photosynthesis in purple phototrophic bacteria. Some species possess the dimeric RC-LH1 complex with a transmembrane polypeptide PufX, representing the largest photosynthetic complex in anoxygenic phototrophs. However, the details of the architecture and assembly mechanism of the RC-LH1 dimer are unclear. Here we report seven cryo-electron microscopy (cryo-EM) structures of RC-LH1 supercomplexes from Rhodobacter sphaeroides. Our structures reveal that two PufX polypeptides are positioned in the center of the S-shaped RC-LH1 dimer, interlocking association between the components and mediating RC-LH1 dimerization. Moreover, we identify another transmembrane peptide, designated PufY, which is located between the RC and LH1 subunits near the LH1 opening. PufY binds a quinone molecule and prevents LH1 subunits from completely encircling the RC, creating a channel for quinone/quinol exchange. Genetic mutagenesis, cryo-EM structures, and computational simulations provide a mechanistic understanding of the assembly and electron transport pathways of the RC-LH1 dimer and elucidate the roles of individual components in ensuring the structural and functional integrity of the photosynthetic supercomplex.

Cryo-EM structure of the photosynthetic RC-LH1-PufX supercomplex at 2.8-Å resolution.

The reaction center (RC)-light-harvesting complex 1 (LH1) supercomplex plays a pivotal role in bacterial photosynthesis. Many RC-LH1 complexes integrate an additional protein PufX that is key for bacterial growth and photosynthetic competence. Here, we present a cryo-electron microscopy structure of the RC-LH1-PufX supercomplex from Rhodobacter veldkampii at 2.8-Å resolution. The RC-LH1-PufX monomer contains an LH ring of 15 αß-polypeptides with a 30-Å gap formed by PufX. PufX acts as a molecular "cross brace" to reinforce the RC-LH1 structure. The unusual PufX-mediated large opening in the LH1 ring and defined arrangement of proteins and cofactors provide the molecular basis for the assembly of a robust RC-LH1-PufX supercomplex and efficient quinone transport and electron transfer. These architectural features represent the natural strategies for anoxygenic photosynthesis and environmental adaptation.