Frequency-Domain Spectroscopic Study of the Photosystem I Supercomplexes, Isolated IsiA Monomers, and the Intact IsiA Ring

Abstract

The PSI 3 −IsiA 18 supercomplex is one of the largest and most complicated assemblies in photosynthesis. The IsiA ring, composed of 18 IsiA monomers (IsiA 18 ) surrounding the PSI trimer (PSI 3 ), forms under iron-deficient conditions in cyanobacteria and acts as a peripheral antenna. Based on the supercomplex structure recently determined via cryo-EM imaging, we model various optical spectra of the IsiA monomers and IsiA 18 ring. Comparison of the absorption and emission spectra of the isolated IsiA monomers and the full ring reveals that about 2.7 chlorophylls (Chls) are lost in the isolated IsiA monomers. The best fits for isolated monomers spectra are obtained assuming the absence of Chl 508 and Chl 517 and 70% loss of Chl 511. The best model describing all three hexamers and the entire ring suggests that the lowest energy pigments are Chls 511, 514, and 517. Based on the modeling results presented in this work, we conclude that there are most likely three entry points for EET from the IsiA 6 hexamer to the PSI core monomer, with two of these entry points likely being located next to each other (i.e., nine entry points from IsiA 18 to the PSI 3 trimer). Finally, we show that excitation energy transfer inside individual monomers is fast (<2 ps at T = 5 K) and at least 20 times faster than intermonomer energy transfer.

High-Resolution Frequency-Domain Spectroscopic and Modeling Studies of Photosystem I (PSI), PSI Mutants and PSI Supercomplexes

“…Over the years, many emission and absorption spectra for the PSI 3 core, PSI 3 -IsiA 18 supercomplexes, and isolated IsiA complexes have been reported [62][63][64]68,158]. Unfortunately, low-temperature optical spectra vary somewhat from one study to another, complicating modeling.…”

“…[158] attributed the observed 685 nm → 682 nm shift in the emission spectra upon switching from the intact ring to a collection of non-interacting IsiA monomers to modified pigment-pigment interactions between the IsiA monomers and a lack of EET among the IsiA monomers and/or to modified interactions between the ring and PSI 3 trimer in the PSI 3 -IsiA 18 supercomplex. However, there were also differences in the absorption and emission spectra of isolated IsiA monomers [62,64,68,158], which might be due to different number of Chls per monomer, as some Chls could be lost during isolation/purification procedures. The latter could lead to different pigment composition of the lowest-energy excitonic states and to shifted emission maxima.…”

“…Reprinted with permission from Ref. [64] Copyright 2022 American Chemical Society. The absorption spectrum of the PSI 3 -IsiA 18 supercomplex shows three maxima located near 670, 676, and 682 nm, as well as an additional weak band near 710 nm.…”

“…It is also possible that this Chl cluster participates in photoprotection. While the B31-B32 dimer or B31-B32-B33 Chl trimer do not focus energy on P700, they may play a role in EET to PSI from the IsiA 18 antenna in a PSI 3 -IsiA 18 supercomplex [64]; see Section 5 for details. The recent structure of the PSI 3 -IsiA 18 supercomplex [124] showed that the predicted lowest-energy Chls of the IsiA ring are likely located close to the B31-B32 dimer.…”

“…We particularly focus on various spectral hole-burning studies [62][63][64][65][66][67][68][69][70][71][72], which are not as common and perhaps not as well appreciated as many of the time-resolved spectroscopies . One can also see this review as a set of examples of what can be done with these methods in photosynthesis research.…”