A team led by Prof. Zhang Yuzhong from the State Key Laboratory of Microbial Technology at Shandong University published a paper entitled “Structural insights into the assembly and energy transfer of haptophyte photosystem I-light-harvesting supercomplex” in Proceedings of the National Academy of Sciences of the United States of America  (PNAS). Prof. Zhang Yuzhong, Prof. Zhao Longsheng, Prof. Liu Luningfrom the University of Liverpool, and Prof. Gao Jun from Huazhong Agricultural University are co-corresponding authors of this paper.

Photosynthesis is the primary process by which light energy is efficiently converted into stable chemical energy in organic matter. It plays a crucial role in providing essential food and nutrients for almost all life forms and maintaining the carbon-oxygen balance of the atmosphere. Photosystem I (PSI) is a multi-subunit pigment-protein complex embedded in thylakoid membranes together with Photosystem II (PSII), which is responsible for capturing and transmitting light energy to drive photosynthetic electron transport. In photosynthetic eukaryotes, the PSI core is surrounded by light-harvesting complex I (LHCI), forming a PSI–LHCI supercomplex that increases the light-trapping cross-section and improves the efficiency of light energy utilization.

Haptophytes are an ecologically important group of single-celled marine phytoplankton that play vital roles as primary producers and have a profound impact on marine ecosystems and global biochemical balance. They are also considered significant in understanding the evolution of photosynthetic phytoplankton.

In this study, the team presents the cryo-electron microscopy structure of the photosystem I–light-harvesting complex I (PSI–LHCI) supercomplex from the haptophyteIsochrysis galbana (Fig 1). The PSI core comprises 12 subunits, which have evolved differently from red algae and cryptophytes by losing the PsaO subunit while incorporating the PsaK subunit, which is absent in diatoms and dinoflagellates. The PSI core is encircled by 22 fucoxanthin-chlorophyll (Chl) a/cproteins (iFCPIs, “i” stands for I. galbana) that form a tri-layered antenna arrangement. Moreover, a pigment-binding subunit, L_iFP, which has not been identified in any other previously characterized PSI–LHCI supercomplexes, was determined in I. galbana PSI–iFCPI, presumably facilitating the interactions and energy transfer between peripheral iFCPIs and the PSI core.

Fig 1 Overall structure of the haptophyte PSI–iFCPI supercomplex

Calculation of excitation energy transfer rates by computational simulations revealed that the intricate pigment network formed within PSI–iFCPI ensures efficient transfer of excitation energy (Fig 2). Haptophyte iFCPIs possess more Chl c than cryptophyte ACPIs and diatom FCPIs. Some of the additional Chls c form efficient energy transfer pathways between iFCPIs in different layers may improve the excitation energy transfer within the specific antenna system of haptophyte PSI–iFCPI.

Fig 2 Excitation energy transfer (EET) pathways in I. galbana PSI–iFCPI

The evolution of red-lineage algae occurred over a billion years ago and involves multiple endosymbiotic events. Plastids originated from primary endosymbiosis when a heterotrophic eukaryotic host engulfed and integrated a cyanobacterium, leading to primary plastids in the first photosynthetic eukaryotes, including red algae, green algae, and glaucophytes. Red algal secondary endosymbiosis led to the diversification of various ecologically important algal groups in modern oceans, such as diatoms, cryptophytes, dinoflagellates, and haptophytes. Structural and phylogenetic analyses indicate that the PSI core and iFCPIs in haptophytes likely have distinct evolutionary origins. The plastid-encoded haptophyte PSI core is thought to be derived from the cryptophyte PSI core, whereas the nuclear-encoded haptophyte iFCPIs are believed to originate from ochrophyte FCPIs (Fig 3).

This study provides a solid structural foundation for understanding the light-harvesting and energy transfer mechanisms in haptophyte PSI–iFCPI and provides insights into the evolution and structural variations of red-lineage PSI–LHCIs.

Fig 3 Possible evolutionary development of red-lineage PSI–LHCI supercomplexes

Prof. Zhang Yuzhong's team has been engaged in the research of algae photosynthesis for decades. This research is a new process in the study of algae photosynthesis following the structure of the photosynthetic membrane of cyanobacteria (Nat Plants, 2020, 6:869; Plant Physiol, 2022, 190:1883), the PSI–LHCI structure of cryptophyte (Plant Cell, 2023, 35:2449), the PSII–LHCII structure of cryptophyte (Nat Commun, 2024,15:4999), and the PSI–LHCI structure of Symbiodinium (Nat Commun, 2024, 15: 2392).

This paper is co-authored by scholars from Shandong University, Ocean University of China, University of Liverpool, and Huazhong Agricultural University. The research is supported by key projects of the National Natural Science Foundation of China and the National Key R&D Program of China.