Unraveling the Evolutionary Trajectory of LHCI in Red-Lineage Algae: Conservation, Diversification, and Neolocalization

Red algae and the secondary symbiotic algae that engulfed a red alga as an endosymbiont are called red-lineage algae. They comprise key marine taxa including diatoms, Haptophyta, and Cryptophyta. Several photosystem (PS) I-light-harvesting complex I (LHCI) structures have been reported from red-lineage algae --two red algae Cyanidioschyzon merolae (Cyanidiophyceae), Porphyridium purpureum (Rhodophytina), a diatom Chaetoceros gracilis and a Cryptophyte Chroomonas placoidea. Here, we clarified the orthologous relation of LHCIs in red-lineage algae by combining a detailed phylogenetic analysis of LHCIs and the structural information of PSI-LHCI. We found that the seven Lhcr groups in LHCI are conserved in Rhodophytina; Furthermore, during both genome reduction in Cyanidioschyzonales of red algae and endosymbiosis leading to Cryptophyta, some LHCIs were lost and replaced by existing or differentiated LHCIs. Especially in Cryptophyta, uniquely diversified Lhcrs form three sets of heterotrimers contributed to the expansion of the antenna size of PSI, supporting the modern ecological success of this taxon. We denominated "neolocalization" to these examples of flexible reorganization of LHCIs. This study provides new insights into the evolutionary process of LHCIs associated with PSI in the red-lineage algae and clarifies the need for both molecular phylogeny and structural information to elucidate the plausible evolutionary history of LHCI.