Crystal structure of plant PSⅠ-LHCⅠ supercomplex and its energy transfer mechanism

Abstract

Photosynthesis uses light energy from the sun to convert CO2 and water into carbohydrates and oxygen, thus sustaining all aerobic life forms on Earth. Energy conversion in photosynthesis is carried out by two large membrane-protein complexes: photosystemⅠ(PSⅠ) and photosystemⅡ(PSⅡ). In higher plants, the PSⅠcore is surrounded by a belt of 4 light-harvestingⅠsubunits (LHCⅠor Lhca), forming a PSⅠ-LHCⅠsupercomplex. The PSⅠ-LHCⅠsupercomplex is an extremely efficient solar energy converter with a quantum efficiency close to 100%. In order to reveal the mechanism of energy harvesting and transfer within this large pigment-protein complex, it is essential to solve its crystal structure. The structure of the PSⅠ-LHCⅠsupercomplex has been analyzed at a resolution up to 3.3 A previously. However, this resolution was not enough to elucidate the detailed mechanism of light-harvesting and energy transfer in this complex. Recently we succeeded in analyzing the structure of the PSⅠ-LHCⅠsupercomplex from pea at 2.8 A resolution (1). Our studies showed that the PSⅠ-LHCⅠsupercomplex contains 16 different subunits (including 12 core subunits PsaA-L and 4 LHCⅠsubunits Lhca1-4) and 205 cofactors (143 chlorophylls a, 12 chlorophylls b, 26 β -carotenes, 5 luteins, 4 violaxanthin, 10 lipids), with a total molecular mass of 600 kD. Our results identified chlorophyll a , chlorophyll b, and some carotenoids in the 4 LHCⅠsubunits for the first time, and revealed the differences in the structures of the 4 LHCⅠ subunits, their interactions, and the interactions between them and the PSⅠcore subunits. Comparison among the available six structures of the Lhc family members (Lhca1 to Lhca4, LHCⅡand CP29) revealed that, although all these Lhc proteins have a highly conserved second protein structure, notable differences were found in the two loop regions AC and BC as well as the N-terminal region. Most pigments are arranged at the same position except some distinct differences among different Lhc subunits in the position of several Chls bound at the interface between adjacent Lhca complexes, and between Lhca and PSⅠcore complex. Based on the structure resolved, 4 plausible energy transfer pathways (1Bs, 1Fl, 2Js, 3As/l) from LHCⅠto the PSⅠcore complex were deduced. Red forms of Chls were found to be involved in energy transfer from each Lhca to PSⅠcore. Our structure revealed that each Lhca binds a red chlorophyll dimer of Chl a 3-Chl a 9, which contribute to red-shifted spectra of Lhca complexes and have a pronounced effect on the energy transfer and trapping in the whole PSⅠ-LHCⅠcomplex. All the four red dimers locate at the interface between LHCⅠand PSⅠcore complex, which looks like four bridges connecting Lhca with the core. The Chl-Chl interactions between each Lhca and the core complex suggested that excitation energy from the LHCⅠbelt to the PSⅠcore would mainly flow via Lhca1 and Lhca3. In this review, we discuss the detailed structure of the PSⅠ-LHCⅠsupercomplex and the possible energy transfer mechanism within it. Taken together, this structure provides a solid structural basis for our understanding on energy transfer and photoprotection mechanisms within PSⅠ-LHCⅠsupercomplex, and thus will be a big step forward toward understanding the mechanisms of photosynthesis.