Structural basis for the adaptation and function of chlorophyll f in photosystem I

Abstract

Chlorophylls (Chl) play pivotal roles in energy capture, transfer and charge separation in photosynthesis. Among Chls functioning in oxygenic photosynthesis, Chl f is the most redshifted type first found in a cyanobacterium Halomicronema hongdechloris. The location and function of Chl f in photosystems are not clear. Here we analyzed the high-resolution structures of photosystem I (PSI) core from H. hongdechloris grown under white or far-red light by cryo-electron microscopy. The structure showed that, far-red PSI binds 83 Chl a and 7 Chl f, and Chl f are associated at the periphery of PSI but not in the electron transfer chain. The appearance of Chl f is well correlated with the expression of PSI genes induced under farred light. These results indicate that Chl f functions to harvest the far-red light and enhance uphill energy transfer, and changes in the gene sequences are essential for the binding of Chl f.

Structure of the far-red light utilizing photosystem I of Acaryochloris

“…2). The overall structure resembles those of PSI trimers reported for other cyanobacteria 1,22,24 . The root-mean-square deviations using secondary structure matching between the monomer model (chains A-M) and Protein Data Bank (PDB) structures 1JB0 of Thermosynechococcus elongatus 1 , 5OY0 of Synechocystis sp.…”

“…The root-mean-square deviations using secondary structure matching between the monomer model (chains A-M) and Protein Data Bank (PDB) structures 1JB0 of Thermosynechococcus elongatus 1 , 5OY0 of Synechocystis sp. PCC 6803 22 , and 6KMX of Halomicronema hongdechloris 24 are 0.90 Å, 0.90 Å, and 0.87 Å, respectively. The A. marina PSI monomer contains 11 subunits [PsaA, PsaB, PsaC, PsaD, PsaE, PsaF, PsaJ, PsaK, PsaL, PsaM, and Psa27], all of which could be assigned to the cryo-EM density map (Fig.…”

Opportunities and challenges for assigning cofactors in cryo-EM density maps of chlorophyll-containing proteins

“…Importantly, two electron density maps obtained by X-ray crystallography can be placed on the same scale so that the maps can be directly compared to identify differences that can be used to reveal missing features. Given the fact that the same scaling cannot be done for ESP maps in cryo-EM, the next best approach is to scale the relative variance of ESP maps, as has only recently appeared in the literature for a protein involved in photosynthesis 3 . However, this approach cannot remove local resolution differences and may be problematic for resolving subtle structural differences as described below.…”

“…The C7 formyl moiety of Chl b is typically found accepting an H-bond from the polypeptide or water, which is thought to confer discrimination against Chl a for specific recognition of Chl b by apo-proteins 28 (see below), as is likely the case for Chl f and d as well. As Chls d and f have been suggested to play roles in electron transfer as well as acting as antenna pigments for FRL absorption in Photosystem I (PSI) and Photosystem II (PSII) 29 , 30 , proteins containing these specialized Chls have been targeted by structural biologists to gain fresh insights in subtle aspects of excitation energy transfer and energy trapping in oxygenic photosynthesis 2 , 3 . Whereas many of these structures are informed by previously determined X-ray crystal structures and their Chls are assigned based on analogy, some recent cryo-EM structures do not have this prior knowledge 2 , 3 and the Chl assignments must be informed instead by direct observation, chemical environment, or energetic constraints, the former of which is a challenge for cryo-EM.…”

High-resolution cryo-EM structure of photosystem II: Effects of electron beam damage

“…The rotational and translational matrix was calculated based on the refined atomic coordinates using lsqkab in CCP4 46 . A map of low-dose PSII was superposed with a map of high-dose PSII which were applied by a low-pass filter and adjusted to 2.08 Å resolution, with calculated rotational and translational matrix using maprot in CCP4 47 . The high-dose PSII map and the low-dose PSII map was normalized based on the ratio of the root mean square map density value and then the difference maps 21 were calculated using UCSF Chimera 37 with the command line option "vop subtract" (Supplementary Fig.…”