During photosynthesis, green algae can absorb light energy through the light-harvesting complexes I and II (LHCI and LHCII) to drive the subsequent processes occurring in photosystems I and II (PSI and PSII). State transitions are a short-term light acclimation mechanism to balance energy distribution between two photosystems. In green algae, state transitions show stronger amplitude and play a wider photoprotective role than those in plants. For example, in Chlamydomonas reinhardtii, the PSI-LHCI-LHCII (CrPSI-LHCI-LHCII) supercomplex is larger and more intricate, and there are nine LhcbM proteins (LhcbM1-9) in four types participating in the formation of LHCII trimers in C. reinhardtii. 

The detailed structure of CrPSI-LHCI-LHCII supercomplex and the subunit composition of LHCII trimers associated with PSI are still unclear. Fundamental questions such as which LhcbM isoforms bind to green algal PSI and how two LHCII trimers establish specific interactions with PSI remain unresolved. The potential excitation energy transfer (EET) pathways between LHCII and PSI-LHCI are to be unraveled at high resolution.

In the study published in Nature Plants on July 8, LI Mei's group and LIU Zhenfeng's group from the Institute of Biophysics (IBP) of the Chinese Academy of Sciences, collaborating with Jun Minagawa's group from National Institutes for Basic Biology, Japan, solved the high-resolution cryo-electron microscopy (cryo-EM) structures of CrPSI-LHCI-LHCII supercomplex.

The researchers discovered that CrPSI-LHCI-LHCII supercomplex is composed of a PSI core. Eight LHCI proteins bound to PSI on one side, two LHCI monomers and two LHCII trimers associated with PSI on the other side, collectively forming a membrane protein-pigment supramolecular complex with an overall molecular weight of about 1,100 kDa.

Based on the high-quality electron microscopy density, they identified the LhcbM proteins involved in the formation of the CrPSI-LHCI-LHCII supercomplex, and that the supercomplex contains all four types of LhcbM proteins. Two specific LhcbM isoforms, namely LhcbM1 and LhcbM5, directly interact with the PSI core through their phosphorylated amino-terminal regions, and LhcbM5 serve as a connector to stabilize the assembly between LhcbM1 and the PSI core.

Furthermore, biochemical and functional studies on mutant strains lacking either LhcbM1 (ΔLhcbM1) or LhcbM5 (ΔLhcbM5) indicated that only LhcbM5 is indispensable for the formation of PSI-LHCI-LHCII supercomplex, and the state transitions in ΔLhcbM5 mutant are affected by the lack of LhcbM5. In the ΔLhcbM1 mutant, LhcbM3 protein replaces LhcbM1 and binds to PSI, thus the supercomplex is still present in this mutant strain.

This study unraveled the specific interactions and potential excitation energy transfer routes between green algal PSI and two phosphorylated LHCIIs in detail, and provided an important foundation for the understanding of the molecular mechanism and evolution of photosynthetic state transitions.