Molecular mechanisms of photoadaptation of photosystem I supercomplex of in an evolutionary cyanobacterial/algal intermediate

The monomeric PSI-LHCI supercomplex from an extremophilic red alga Cyanidioschyzon merolae represents an intermediate evolutionary link between the cyanobacterial PSI reaction centre and its green algal/higher plant counterpart. We show that the C. merolae PSI-LHCI supercomplex is characterized by robustness in various extreme conditions. By combination of biochemical, spectroscopic, mass spectrometry and electron microscopy/single particle analyses we dissected three molecular mechanisms underlying inherent robustness of C. merolae PSI-LHCI supercomplex: (i), the accumulation of a photoprotective zeaxanthin in the LHCI antenna and the PSI reaction centre; (ii), structural remodelling of the LHCI antenna and adjustment of its effective absorption cross-section; and (iii), dynamic re-adjustment of the stoichiometry of the two PSI-LHCI isomers and changes in the oligomeric state of the PSI-LHCI supercomplex, accompanied by dissociation of the PsaK core subunit. We show that the largest low light-treated C. merolae PSI-LHCI supercomplex can bind up to 8 Lhcr antenna subunits which are organized as 2 rows on the PsaF/PsaJ side of the core complex. Under our experimental conditions, we found no evidence of functional coupling of the phycobilisomes with the PSI-LHCI supercomplex purified from various light conditions, suggesting that the putative association of this antenna with PSI supercomplex is absent or transient, or may be lost during the purification procedure.