A team led by Prof. Zhang Yuzhong from the State Key Laboratory of Microbial Technology at Shandong University published a paper entitled "Structure of cryptophyte photosystem II–light-harvesting antennae supercomplex" in Nature Communications. Prof. Zhang Yuzhong, Prof. Zhao Longsheng, Prof. Liu Luning from the University of Liverpool, and Prof. Gao Jun from the Huazhong Agricultural University are co-corresponding authors of this paper.

Oxygen-releasing photosynthesis is one of the most important life processes on Earth, producing oxygen and organic matter and playing an important role in driving the evolution of life. Cyanobacteria, eukaryotic algae and land plants convert light energy into chemical energy through oxygen-releasing photosynthesis, which supplies almost all life activities on Earth. The light energy conversion depends on the precise coordination of various photosynthetic complexes on the photosynthetic membrane and free electron transport carriers. PSII is a key complex responsible for photosynthetic electron transfer, composed of many protein subunits and a large number of pigments, which can absorb light energy and catalyze water cracking to produce electrons, protons and oxygen, and is one of the most important biochemical reactions on Earth. The analysis of the structure of PSII is crucial to elucidate its mechanism of light energy capture, transfer and conversion.

Cryptophyte is an important phylum in red-lineagealgae. It is widely distributed, an important primary producer, and has important ecological functions. Cryptophyte is an ancient group derived from red algae. Unlike red algae PSII, cryptophyte PSII associates with transmembrane LHC and forms PSII–LHCII supercomplex for the first time in red-lineage algae. We speculate that cryptophyte PSII–LHCII may have a unique structure and light energy capture and transfer mechanism, and it may represent the intermediate state of PSII structure evolution in red-lineage algae, and its LHCII may have the same origin as LHCI, both evolved from red alga LHCR.

In this study, we present the cryo-electron microscopy structure of the Photosystem II (PSII)–ACPII supercomplex from the cryptophyte Chroomonas placoidea. (Fig. 1). Its unique LHCII binding mode, pigment network, and energy transfer mechanism were elucidated. The structural evolution of PSII and the origin of LHCII were revealed. cryptophyte PSII–LHCII consists of a dimeric core and 12 LHCII. The linear trimers of LHCII are similar to those of red algalLHCI and cryptophyte LHCI. Combined with phylogenetic analysis, the close evolutionary relationship between LHCII and cryptophyte LHCI is indicated. In addition, the structure contains a cryptophyte-specific subunit Psb-γ, which contains chlorophyll and binds with LHCII to stabilize the structure of PSII–LHCII.

Fig. 1. Atomic structure of the PSII–LHCII supercomplexfromcryptophyte

Due to the special arrangement of cryptophyte LHCII and the new pigment sites, cryptophyte PSII–LHCII forms a unique pigment network and energy transfer pathway. Cryptophytes and diatoms have different LHCII arrangements and pigment compositions, which may provide the basis for cryptophytes and diatoms to survive in their specific ecological niches.

Cryptophyte PSII-LHCII not only has the characteristics of red algalPSII and diatom PSII–LHCII but also has its own characteristics. The structural similarities and differences of the three PSII supercomplexes indicate that the structure of cryptophyte PSII–LHCII is in an intermediate state between red algae and diatoms, which is consistent with the structural evolution analysis of its PSI–LHCI (Fig. 2). Structural analysis and phylogenetic analysis showed that cryptophytes LHCII evolved fromitsLHCI, both originated from red algal LHCI. This study lays a solid structural foundation for understanding the mechanism of light energy capture and energy transfer of cryptophyte PSII-LHCII, reveals the evolution of PSII–LHCII and the origin of transmembrane LHCII in red-lineagealgae, and improves the structural evolution process of PSII-LHCII.

Fig. 2. Speculated evolution process of PSII–LHCII structure: red algae-cryptophyte-diatom

Prof. Zhang Yuzhong's group 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) 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, Qingdao Marine Science and Technology Center and Huazhong Agricultural University. The research is supported by the Key Program of the National Natural Science Foundation of China and the National Key R&D Program of China.

The original link of the paper is https://doi.org/10.1038/s41467-024-49453-0.