Physiological and Evolutionary Implications of Tetrameric Photosystem I in Cyanobacteria

Abstract

words): 1Photosystem I (PSI) were reported as trimeric complexes in most characterized 2 cyanobacteria, yet monomers in plants and algae PSI. Recent reports on tetrameric PSI 3 raised questions regarding its structural basis, physiological role, phylogenetic distribution 4 and evolutionary significance. In this study, by examining PSI in 61 cyanobacteria, we 5show that tetrameric PSI, correlating with a unique psaL gene and genomic structure, is 6 widespread in the heterocyst-forming cyanobacteria and their close relatives. Physiological 7 studies on these cyanobacteria revealed that tetrameric PSI is favored under high light, with 8 an increased content of novel PSI-bound carotenoids (myxoxanthophyll, canthaxanthan 9 and echinenone). Together this work suggests that tetrameric PSI is an adaptation to high 10 light, along with results showing that change in PsaL leads to trimeric PSI monomerization, 11 supporting the hypothesis of tetrameric PSI being the evolutionary intermediate in the 12 transition from cyanobacterial trimeric PSI to monomeric PSI in plants and algae. 13 15 2011; Watanabe et al., 2014) and Chroococcidiopsis sp. TS-821 (TS-821) (Li et al., 2014; 35 Semchonok et al., 2016; Shelaev et al., 2018) challenged this preconceived notion of PSI trimer 36 being the sole oligomer in cyanobacteria. Yet, the PSI tetramer has not been viewed as a major 37 oligomeric state in cyanobacteria. Although the discovery of tetrameric PSI in two species is 38 now accepted, the mechanism controlling the oligomeric assembly and stability is not known. 39 Furthermore, the physiological and evolutionary significance of this structural change has yet to 40 be elucidated. A recent cryo-EM structure of PSI tetramer from TS-821 showed that tetrameric 41 PSI is actually a dimer of dimers with two different interaction interfaces between monomers 42 (Semchonok et al., 2016). This structure suggests subtle changes in the placement of the central 43 subunit PsaL, yielding changes in helical bundling that has been implicated to be critical in the 44 formation of PSI trimers. 45 S2u). However, Nostoc sp. PCC 9335 represents the only species of cyanobacteria observed that 77 had significant amounts of both trimeric and dimeric forms of PSI ( Fig. S3a). Analysis of the 78 unicellular cyanobacteria that are closely related to the heterocyst-forming cyanobacteria (Shih et 79 al., 2013) including TS-821, Synechocystis sp. PCC 7509 and Gloeocapsa sp. PCC 7428 ( Fig. 80 S2a, b), exhibit more tetrameric, dimeric, and monomeric PSI than trimeric PSI. The two other 81species of Chroococcidiopsis that we tested, Chroococcidiopsis thermalis PCC 7203 (Fig. 1a, c) 82 and Chroococcidiopsis sp. PCC 7434 (Fig. S3a), contained primarily monomeric PSI with some 83 dimeric PSI. Collectively, these results revealed that besides monomeric PSI, tetrameric and 84 dimeric PSI, instead of trimeric PSI, comprise the majority of PSI oligomers in the HCR. 85Trimeric PSI was either not detectable or only present as a minor species in this clade (Dat...