Recent advances in the structural diversity of reaction centers

Abstract

Photosynthetic reaction centers (RC) catalyze the conversion of light to chemical energy that supports life on Earth, but they exhibit substantial diversity among different phyla. This is exemplified in a recent structure of the RC from an anoxygenic green sulfur bacterium (GsbRC) which has characteristics that may challenge the canonical view of RC classification. The GsbRC structure is analyzed and compared with other RCs, and the observations reveal important but unstudied research directions that are vital for disentangling RC evolution and diversity. Namely, (1) common themes of electron donation implicate a Ca2+ site whose role is unknown; (2) a previously unidentified lipid molecule with unclear functional significance is involved in the axial ligation of a cofactor in the electron transfer chain; (3) the GsbRC features surprising structural similarities with the distantly-related photosystem II; and (4) a structural basis for energy quenching in the GsbRC can be gleaned that exemplifies the importance of how exposure to oxygen has shaped the evolution of RCs. The analysis highlights these novel avenues of research that are critical for revealing evolutionary relationships that underpin the great diversity observed in extant RCs.

Structure of a monomeric photosystem II core complex from a cyanobacterium acclimated to far-red light reveals the functions of chlorophylls d and f

“…This configuration is reminiscent of a “bump-and-hole” strategy used in protein engineering efforts to confer cofactor specificity to study enzyme–substrate interactions ( 66 ). It is also reminiscent of a recent cryo-EM structure of the PSI-like photochemical reaction center from the anoxygenic chlorophototroph, Chlorobaculum tepidum , which uses bacteriochlorophyll a as its major antenna pigment ( 67 ) but confers specificity to ETC sites to bind Chl a by steric hindrance near the C3 position ( 68 ). The unique coordination of the Chl f at PsbB2-605 may be related to its position, somewhat overlapping with the Chl f at site PsbB2-614.…”

Shedding Light on Primary Donors in Photosynthetic Reaction Centers

“…Examination of the primary donor of the GsbRC in Figure 8F reveals that the protein-matrix effects are much more pronounced than those of the analogous homodimeric RC, the HbRC, from H. modesticaldum. As discussed recently, the markedly lower resolution of the cryo-electron microscopy structure (as compared to other X-ray structures) suggests that assignments of protein matrix interactions should be considered tentative (Gisriel et al, 2021). There exists a total of four hydrogen bonds, two on each BChl macrocycle, provided by the Tyr681 and Thr685 residues (Figure 8F).…”

Origin and Early Evolution of Photosynthesis: A Brief Historical Account

“…The second water bound to the Ca in the HbRC also overlaps with a water molecule bound to the Ca in the water-oxidizing cluster known as 'W4' (not shown for clarity). Other striking similarities are described in and see also Gisriel et al (2021). D1-Y126 (PSII) and PshA-F339 (HbRC) occupy homologous position, but Y126 provides a hydrogenbond to PhD1.…”

“…In the HbRC the interaction with an equivalent carotenoid is replaced by an interaction with a lipid. It suggests that this position has been under pressure to enhance photoprotection from excess excitation from early on (Gisriel et al 2021). D These structural relationships show that the "architecture of photosystem II" is not only ancestral to type II reaction centres, but it is also required and optimized to catalyse and sustain water oxidation.…”