Structure of a symmetric photosynthetic reaction center–photosystem

Abstract

Reaction centers are pigment-protein complexes that drive photosynthesis by converting light into chemical energy. It is believed that they arose once from a homodimeric protein. The symmetry of a homodimer is broken in heterodimeric reaction-center structures, such as those reported previously. The 2.2-angstrom resolution x-ray structure of the homodimeric reaction center-photosystem from the phototroph exhibits perfect symmetry. The core polypeptide dimer and two small subunits coordinate 54 bacteriochlorophylls and 2 carotenoids that capture and transfer energy to the electron transfer chain at the center, which performs charge separation and consists of 6 (bacterio)chlorophylls and an iron-sulfur cluster; unlike other reaction centers, it lacks a bound quinone. This structure preserves characteristics of the ancestral reaction center, providing insight into the evolution of photosynthesis.

Early Archean origin of Photosystem II

“…The acquisition of closely interacting carotenoids seems to have occurred therefore after the K and D0 divergence, but before the D1 and D2 split, in support of water oxidation before heterodimerization. However, carotenoids at a similar position to Car D1 and Car D2 have recently been identified in the homodimeric Type I reaction center of Heliobacteria (Gisriel et al, 2017) suggesting that these may predate the Type I/Type II split (Figure 8).…”

“…Unlike neurotoxins, photosynthetic reaction centers are highly regulated large multisubunit membrane protein complexes binding dozens of cofactors at precise orientations and distances to allow efficient photochemistry to occur. Even the “simplest” known homodimeric reaction center is made of at least four protein subunits binding 62 chlorophyll‐derived pigments, two carotenoids, two lipids, four Ca 2+ ions, and a Fe 4 S 4 cluster (Gisriel et al., ). It is therefore likely that reaction centers have always been under strong purifying selection (Shi, Bibby, Jiang, Irwin, & Falkowski, ).…”

“…The role of this carotenoid is to quench bacteriochlorophyll triplet states to prevent the formation of singlet oxygen (Cogdell et al., ). A carotenoid with a similar position to Car D1 and Car D2 in PSII has been now discovered in the structure of a homodimeric Type I reaction center (Gisriel et al., ). In addition, light‐harvesting complexes in all anoxygenic photosynthetic bacteria contain carotenoids (e.g., chlorosome, LH1, LH2, B808‐866), which perform photoprotective roles (Kim, Li, Maresca, Bryant, & Savikhin, ; Melo, Frigaard, Matsuura, & Naqvi, ; Tsukatani, Romberger, Golbeck, & Bryant, ).…”

“…TA B L E 3 Comparison of rates of protein evolution to occur. Even the "simplest" known homodimeric reaction center is made of at least four protein subunits binding 62 chlorophyll-derived pigments, two carotenoids, two lipids, four Ca 2+ ions, and a Fe 4 S 4 cluster (Gisriel et al, 2017). It is therefore likely that reaction centers have always been under strong purifying selection (Shi, Bibby, Jiang, Irwin, & Falkowski, 2005).…”

Reduced sulphur sources favour HgII reduction during anoxygenic photosynthesis by Heliobacteria

“…Heliobacteria are metabolically versatile terrestrial spore forming photoheterotrophs that also conduct one of the most primitive forms of photosynthesis. They are used to study the function of ancestral photochemical reaction centres, the key components in the energy conversion process of photosynthesis (Gisriel et al, 2017;Orf, Gisriel, & Redding, 2018). Determining their role on Hg redox transformations is not only relevant for contemporary environments, but may also provide insights into the chemistry of early Earth by identifying conditions that may leave a redox-mediated signature in the rock record (Zheng, Gilleaudeau, Kah, & Anbar, 2018).…”