Structure of the Acidobacteria homodimeric reaction center bound with cytochrome c

Abstract

Photosynthesis converts light energy to chemical energy to fuel life on earth. Light energy is harvested by antenna pigments and transferred to reaction centers (RCs) to drive the electron transfer (ET) reactions. Here, we present cryo-electron microscopy (cryo-EM) structures of two forms of the RC from the microaerophilic Chloracidobacterium thermophilum (CabRC): one containing 10 subunits, including two different cytochromes; and the other possessing two additional subunits, PscB and PscZ. The larger form contained 2 Zn-bacteriochlorophylls, 16 bacteriochlorophylls, 10 chlorophylls, 2 lycopenes, 2 hemes, 3 Fe4S4 clusters, 12 lipids, 2 Ca2+ ions and 6 water molecules, revealing a type I RC with an ET chain involving two hemes and a hybrid antenna containing bacteriochlorophylls and chlorophylls. Our results provide a structural basis for understanding the excitation energy and ET within the CabRC and offer evolutionary insights into the origin and adaptation of photosynthetic RCs.

Experimental and Theoretical Mutation of Exciton States on the Smallest Type-I Photosynthetic Reaction Center Complex of a Green Sulfur Bacterium Chlorobaclum tepidum

“…Thus, multiple type-I RCs seem to have adapted to diverse light environments using different species and numbers of pigments bound to homologous protein architectures. This situation is essentially similar to the recently identified structure of the unique type-I RC of Acidobacterium, which contains BChl a , Chl a , and a special pair of Zn-containing BChl a molecules on the homodimer of the two PscA-like polypeptides . Therefore, it would be interesting to determine the rules and evolution of the molecular architecture of type-I RCs based on the revealed RC structures using modern quantum mechanical theory.…”

“…This situation is essentially similar to the recently identified structure of the unique type-I RC of Acidobacterium, which contains BChl a, Chl a, and a special pair of Zn-containing BChl a molecules on the homodimer of the two PscA-like polypeptides. 11 Therefore, it would be interesting to determine the rules and evolution of the molecular architecture of type-I RCs based on the revealed RC structures using modern quantum mechanical theory. GsbRC (Figure 1), which binds the smallest number of pigments among type-I RCs, appears to remain a feature of the prototype type-I RC that is still unknown.…”

“…Recent structural analyses have also contributed to theoretical studies on the physical processes occurring within type-I RCs. ,,,,− Adolphs et al calculated the excitonic coupling strength between every pair of Chl a molecules on PSI using the Poisson TrESP (P-TrESP) method and obtained the spatial distribution of the site energy shift (SES) values using the charge density coupling (CDC) method. SES values indicate the differences in the electrostatic interactions between the excited and ground states of the Chl a molecules and the surrounding polypeptides.…”

Recognition of histidines with a synthetic zinc amino‐oxochlorin regioisomer via synergetic coordination and hydrogen bonding

“…Chlorophylls (Chls) are essential for the initial stage of photosynthesis and play important roles in light absorption/harvesting, excitation energy transfer, and charge separation. Chl pigments usually interact with peptides to form the above functionalized apparatuses in photosynthetic organisms 1–14 except for their self‐aggregates in specific antenna systems 15 . In the proteins, the central magnesium atoms in Chl molecules are ligated by a variety of species including peptidyl residues to give the five‐coordinated complexes.…”

“…The histidyl imidazolyl group is primarily utilized as the axial ligand, while the residues of aspartic/glutamic acids, asparagine/glutamine, tyrosine, and methionine coordinate to the Mg atoms 16 . In a chloracidobacterium as one of the photosynthetic bacteria, the central zinc atom of a Chl pigment is coordinated with a nitrogen atom of the imidazolyl group in the neighboring histidine 12 . All the Chls are fixed in the protein matrices by the coordination to the central metals.…”