Unique organization of photosystem I–light-harvesting supercomplex revealed by cryo-EM from a red alga

Abstract

Photosystem I (PSI) is one of the two photosystems present in oxygenic photosynthetic organisms and functions to harvest and convert light energy into chemical energy in photosynthesis. In eukaryotic algae and higher plants, PSI consists of a core surrounded by variable species and numbers of light-harvesting complex (LHC)I proteins, forming a PSI-LHCI supercomplex. Here, we report cryo-EM structures of PSI-LHCR from the red alga in two forms, one with three Lhcr subunits attached to the side, similar to that of higher plants, and the other with two additional Lhcr subunits attached to the opposite side, indicating an ancient form of PSI-LHCI. Furthermore, the red algal PSI core showed features of both cyanobacterial and higher plant PSI, suggesting an intermediate type during evolution from prokaryotes to eukaryotes. The structure of PsaO, existing in eukaryotic organisms, was identified in the PSI core and binds three chlorophylls and may be important in harvesting energy and in mediating energy transfer from LHCII to the PSI core under state-2 conditions. Individual attaching sites of LHCRs with the core subunits were identified, and each Lhcr was found to contain 11 to 13 chlorophylls and 5 zeaxanthins, which are apparently different from those of LHCs in plant PSI-LHCI. Together, our results reveal unique energy transfer pathways different from those of higher plant PSI-LHCI, its adaptation to the changing environment, and the possible changes of PSI-LHCI during evolution from prokaryotes to eukaryotes.

Structural features of the diatom photosystem II–light‐harvesting antenna complex

“…These deviations may result from the different lengths of the FCP polypeptides and their distinctly different locations, which may confer them different roles in energy harvesting and transfer. A similar situation can be found in LHCII and LHCI in the green lineage organisms, where different numbers of Chls a and b , and slightly different bindings sites of Chls, are also found .…”

“…To understand the oligomeric state, organization of protein subunits, and the exact composition and distribution of pigments and other cofactors in the PSII core and its complex with antenna proteins, several PSII structures from cyanobacteria, red alga, green alga, and higher plants have been solved by cryo‐electron microscopy (cryo‐EM) and X‐ray crystallography . In particular, single‐particle cryo‐EM analysis has provided a powerful tool to unravel the organization of several PSII–LHC and PSI–LHC supercomplexes from different lineages of organisms from cyanobacteria to green algae and higher plants . The structure of PSII–FCPII from diatoms, however, was solved only recently , and a high‐resolution crystal structure of an isolated FCP dimer was also reported recently .…”

Isolation and characterization of CAC antenna proteins and photosystem I supercomplex from the cryptophytic alga Rhodomonas salina

“…Looking at the pigment data (Table ), it is possible to get an estimate of the pigment composition of PSI antenna, built on the assumption that R. salina PSI core , like all known PSI cores, binds approximately 20 carotenes +100 Chl a . For instance, utilizing red‐algal PSI core value of 21 + 97 (Pi et al ) after normalizing to carotene, one gets approximately 230 Chl a per PSI supercomplex, a standard value for PSI supercomplexes from a broad phylogenetic range, from red algae, heterokonts to green algae (Kargul et al , Ikeda et al , Thangaraj et al , Bína et al ). The pigment content of PSI antenna can then be computed by the difference (Table ).…”

“…Estimated pigment content per PSI core of the PSI supercomplex and PSI antenna calculated using measured values taken fromTable 2(shaed lines) and assuming 97 Chl a and 21 carotene molecules per PsaA/B dimer (see, e.g Pi et al 2018…”

Integration of a Galdieria plasma membrane sugar transporter enables heterotrophic growth of the obligate photoautotrophic red alga Cynanidioschyzon merolae

“…Thus far, this alga has facilitated studies on cell cycle (Fujiwara, Tanaka, Kuroiwa, & Hirano, 2013;Kobayashi et al, 2009;Miyagishima et al, 2014), division and inheritance of organelles (Imoto et al, 2018;Miyagishima et al, 2003;Yagisawa, Nishida, Kuroiwa, Nagata, & Kuroiwa, 2007;Yoshida et al, 2017), and nitrogen and carbohydrate metabolism (Imamura et al, 2009;Pancha et al, 2018). In addition, there have been recent biochemical, spectroscopic, and high-resolution structural studies of photosystems in this alga (Antoshvili, Caspy, Hippler, & Nelson, 2018;Busch, Nield, & Hippler, 2010;Krupnik et al, 2013;Pham, Janna Olmos, Chernev, Kargul, & Messinger, 2018;Pi et al, 2018).…”