Chapter 12 - The structural diversity of bacterial reaction center-light harvesting 1 complexes and their role in developing biohybrid photoelectrochemical cells

Abstract

The reaction center (RC)-light harvesting 1 (LH1) core complex plays a central role in anoxygenic photosynthesis by harvesting radiant energy funneled to the RC bacteriochlorophyll (BChl) special pair where a transmembrane charge separation is initiated that results in the gated reduction of quinone (Q) molecules. The resulting quinol is translocated to the cytochrome bc1 complex, generating an electrochemical proton gradient driving ATP synthesis. The 1.9Å X-ray structure of RC-LH1 from the purple sulfur bacterium Thermochromatium tepidum (Yu et al. Nature 556:209–213, 2018) showed that strong interactions between the 16 Ca2+ ions and the 16 αβ-LH1 heterodimeric subunits largely accounted for thermal stability and the extended redshift of the LH1 QY-absorption band. In addition to the ubiquinone (UQ) and menaquinone molecules in their respective QB and QA sites, the RC contained four additional UQs engaged in exchange pathways via passage through narrow pore(s) between LH1 subunits. A unique diacylglycerol and N-terminal Cys linkage anchoring the c-type cytochrome RC component to the membrane was also revealed. Due to major recent advancements in single particle cryo-electron microscope analysis, the structures of the RC-LH1 complexes from six additional purple bacterial species have been determined, as well as for the mosaic LH-RC complex from a filamentous anoxygenic phototroph. The 2.8-Å structure for the Ca2+-containing RC-LH1 complex of the mesophilic Thiorhodovibrio strain 970 also contained a closed ring of 16 subunits with 32 BChl a molecules (Tani et al., Nature Commun. 11:4955, 2020). A Ca2+-enhanced network of H-bonds accounted for the large redshift of the LH1 QY-BChl a absorption band, while the distribution of multiple isoforms of the α- and β-protomers within the LH1 ring structure was also revealed. The 2.5Å structure of the 16-membered Rhodospirillum rubrum LH1 ring containing core complex (Qian et al., Biochem. J. 478:3253–3263, 2021) showed a third monomeric RC BChl as well as an accessory Q molecule (QP) in the same position as a Tch. tepidum Q molecule, reflecting a common Q diffusion mechanism through the LH1 ring. For the 2.9-Å BChl b-containing Blastochloris viridis core complex structure (Qian et al., Nature 556:203–208, 2018), a single αβ-heterodimer was found together with 16 αβγ-heterotrimers; an LH1 opening sufficient for Q exchange was created by the missing γ-subunit. Tight γ-subunit packing and shortened distances between BChl pairs were thought to contribute to the large LH1 QY-BChl b redshift. In Rhodobacter sphaeroides, where fused 14-membered rings form an S-shaped dimer, a 2.9- Å structure (Qian et al., Biochem. J. 478:3923–3937, 2021) revealed two previously unrecognized proteins (-Y and -Z) adjacent to the ring opening, which together with PufX participate in formation of the Q-redox species exchange gap. A pivotal role in ring dimerization was attributed to the presence of sulfoquinovosyl diglyceride. Likely participating Q-exchange species were observed in the respective 15- and 14-membered open ring structures from Rba. veldkampii (Bracun et al., Sci. Adv. 7:eabf8864, 2021) and Rhodopseudomonas palustris (Swainsbury et al., Sci. Adv. 7:eabe2631, 2021) determined at 2.8 and 2.9Å resolution. An open RC-LH complex was also seen in the 4.1Å structure for the filamentous anoxygenic phototroph Roseiflexus castenhlozii (Xin et al., Nature Commun. 9:1568, 2018) where a Q channel was created by incorporation into the LH ring of the anchoring cytochrome c helix and the newly described protein X. Owing to extensive research efforts over the past several years, the RC-LH1 complex has become an important component in the development of biohybrid photoelectrochemical cells. It is now apparent that these endeavors represent a crucial demonstration of the photoexcitation properties of a biological system for efficient harvesting and transduction of radiant energy in a solid-state device that can be successfully implemented as a functional solar cell.