Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana

Abstract

Summary Photosystem I (PSI) is a pigment protein complex catalyzing the light‐driven electron transport from plastocyanin to ferredoxin in oxygenic photosynthetic organisms. Several PSI subunits are highly conserved in cyanobacteria, algae and plants, whereas others are distributed differentially in the various organisms.Here we characterized the structural and functional properties of PSI purified from the heterokont alga Nannochloropsis gaditana, showing that it is organized as a supercomplex including a core complex and an outer antenna, as in plants and other eukaryotic algae.Differently from all known organisms, the N. gaditana PSI supercomplex contains five peripheral antenna proteins, identified by proteome analysis as type‐R light‐harvesting complexes (LHCr4‐8). Two antenna subunits are bound in a conserved position, as in PSI in plants, whereas three additional antennae are associated with the core on the other side. This peculiar antenna association correlates with the presence of PsaF/J and the absence of PsaH, G and K in the N. gaditana genome and proteome.Excitation energy transfer in the supercomplex is highly efficient, leading to a very high trapping efficiency as observed in all other PSI eukaryotes, showing that although the supramolecular organization of PSI changed during evolution, fundamental functional properties such as trapping efficiency were maintained.

Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans

“…refs 2 , 3 ). There are also differences in numbers of small subunits; red algal-derived plastids, for example, lack PsaG and PsaH subunits 4 . The evolution of eukaryotic (plastid) PSI also eliminated the oligomeric (trimeric) form of PSI common in cyanobacteria; plastid PSIs are typically monomeric 5 .…”

“…The number of taxa where the differences in photosystem protein composition have been examined and compared is relatively small – studies have been confined mostly to higher plants, Chlamydomonas , and cyanobacteria, although research has recently extended to red algae and stramenopiles 4 , 9 – 13 . Considering the tremendous diversity of photosynthetic organisms and the complexity of plastid evolution in eukaryotes, our current understanding of photosystem composition is extremely limited.…”

Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K

“…(B) The 77 K fluorescence emission spectrum of isolated PSII from Nannochloropsis oceanica (excitation wavelength 435 nm) (Litvín et al 2016). (C) The 77 K fluorescence emission spectrum of isolated PSI-LHC complexes isolated from Nannochloropsis gaditana (mainly dimeric: black, mainly monomeric: blue) (Alboresi et al 2017) and PSI-supercomplex (red) (Litvín et al 2016…”

“…Panels A and B were digitized from Litvín et al (2016). (C) was digitized from Alboresi et al (2017). use predominantly the carotenoids violaxanthin and vaucheroaxanthin as light-harvesting pigments and for photoprotection. Chl a and the carotenoids are housed in LHCs, called VCP for viola-/vaucheriaxanthin Chl protein (Fig.…”

Composition, phosphorylation and dynamic organization of photosynthetic protein complexes in plant thylakoid membrane

“…73,74 The fact that the Lhca proteins form dimers while the Lhcb proteins preferentially oligomerize as trimers likely derives from the slightly different orientation of their N-terminus. 70 It is important to note that, despite the highly conserved PSI-LHCI complex with four Lhca proteins, some species diverge from this model by dividing the Lhca proteins between the PsaF and the PsaH side 75 or by binding additional Lhca proteins on the PsaH 76 or PsaF 77 side of the PSI core. Interestingly, an additional Lhca1/Lhca4 dimer bound to PsaH side was recently found in Arabidopsis.…”