The structure of a red-shifted photosystem I reveals a red site in the core antenna

Abstract

Photosystem I coordinates more than 90 chlorophylls in its core antenna while achieving near perfect quantum efficiency. Low energy chlorophylls (also known as red chlorophylls) residing in the antenna are important for energy transfer dynamics and yield, however, their precise location remained elusive. Here, we construct a chimeric Photosystem I complex in Synechocystis PCC 6803 that shows enhanced absorption in the red spectral region. We combine Cryo-EM and spectroscopy to determine the structure−function relationship in this red-shifted Photosystem I complex. Determining the structure of this complex reveals the precise architecture of the low energy site as well as large scale structural heterogeneity which is probably universal to all trimeric Photosystem I complexes. Identifying the structural elements that constitute red sites can expand the absorption spectrum of oxygenic photosynthetic and potentially modulate light harvesting efficiency.

Excitation energy transfer kinetics of trimeric, monomeric and subunit-depleted Photosystem I from Synechocystis PCC 6803

“…is not the longest-wavelength form but emits at 713 nm in the trimeric PSI. The same three sites have been recently assigned as red Chls in Synechocystis PCC 6803 absorbing at 706, 707 and 714 nm [24,62]. We tentatively set the same absorption wavelengths (see Supplementary table S4), which resulted in an excellent fit of the experimental 77 K absorption and emission spectra (Supplementary Figure S8).…”

“…The lowest-energy states emitting at 722-724 nm remain to be located on one or more Chls outside the monomerization region, e.g. A38/A39, B31/B32, B37/B38 [23][24][25]54].…”

“…Deconvolution analyses of the absorption spectra of PSI of Synechocystis PCC 6803 [18] and spectral holeburning studies [19,20] have indicated that ~5 red Chls are present in trimers and ~3 in monomers. It has been recognized that the red forms originate from strong Coulombic interactions between the Chls and several candidate pigments (or pigment groups) have been proposed [4,[21][22][23][24][25][26], but these assignments remain largely hypothetical.…”

Cryo-EM structure of a functional monomeric Photosystem I from Thermosynechococcus elongatus reveals red chlorophyll cluster

“…7 ). In a very recent study, a chimeric Synechocystis PCC 6803 PSI into which the lumenal PsaB loop supporting the outer staircase chlorophyll B1233 was introduced has been characterized by both cryo-EM and spectroscopy 21 . The cryo-EM based atomic model showed that an additional chlorophyll corresponding to B1233 is present in the chimeric PSI complex and is causing a red shift.…”

“…However, to date, with a notable exception of the PSI monomer structure from Synechocystis sp. PCC 6803 solved at 4.0 Å resolution by X-ray crystallography 14 , all structures of cyanobacterial PSI have been determined from trimeric complexes 8,[15][16][17][18][19][20][21] or the recently discovered tetrameric PSI from Anabaena sp. PCC 7120 [22][23][24] and Chroococcidiopsis sp.…”