Structural basis for blue-green light harvesting and energy dissipation in diatoms

Abstract

Diatoms are abundant photosynthetic organisms in aquatic environments and contribute 40% of its primary productivity. An important factor that contributes to the success of diatoms is their fucoxanthin chlorophyll a/c-binding proteins (FCPs), which have exceptional light-harvesting and photoprotection capabilities. Here, we report the crystal structure of an FCP from the marine diatom Phaeodactylum tricornutum, which reveals the binding of seven chlorophylls (Chls) a, two Chls c, seven fucoxanthins (Fxs), and probably one diadinoxanthin within the protein scaffold. Efficient energy transfer pathways can be found between Chl a and c, and each Fx is surrounded by Chls, enabling the energy transfer and quenching via Fx highly efficient. The structure provides a basis for elucidating the mechanisms of blue-green light harvesting, energy transfer, and dissipation in diatoms.

Structural features of the diatom photosystem II–light‐harvesting antenna complex

“…However, this motif is absent in FCPs, and characteristic monomer–monomer interactions within the FCP‐A tetramer are found between pigment–pigment and pigment–proteins at both stromal and lumenal sides . These interactions are different from those found in the dimeric FCP and trimeric LHCII, thus illustrating the different oligomerization states and high flexibility of the protein subunits in the LHC superfamily , which may be a result of adaptation to fulfill their roles for light harvesting and photoprotection in different light environments.…”

“…According to the symmetry of their siliceous cell walls, diatoms are divided into two groups, namely pennate and centric groups. Genome and peptide analyses show that the pennate and centric diatoms have different composition of Lhcf subunits in thylakoid membranes . In the centric diatom Chaetoceros gracilis , FCPII exists mainly in three types designated FCP‐A, FCP‐B, and FCP‐C .…”

“…The detailed binding environments of Chls c and Fxs in FCP are visualized from a higher resolution (1.8 Å) structure of an isolated FCP subunit from a pennate diatom P. tricornutum analyzed by X‐ray crystallography . This structure showed that the isolated FCP exists in a dimeric form (Fig.…”

“…The main state of FCPIIs around PSII core is previously suggested as trimer based on the LHCII trimer structure of green lineage organisms . However, we isolated a homodimeric FCP from a pennate diatom Phaeodactylum tricornutum and solved its crystal structure at a high resolution . This dimer is encoded by an lhcf4 gene and may be one of the important forms of FCP existing around the PSII core.…”

“…In particular, single‐particle cryo‐EM analysis has provided a powerful tool to unravel the organization of several PSII–LHC and PSI–LHC supercomplexes from different lineages of organisms from cyanobacteria to green algae and higher plants . The structure of PSII–FCPII from diatoms, however, was solved only recently , and a high‐resolution crystal structure of an isolated FCP dimer was also reported recently . These studies revealed the oligomeric states and organization of FCPII subunits around the PSII core, the distribution and detailed binding environments of Chls c and Fxs, and a huge pigment–protein network within the PSII–FCPII supercomplex, which enable us to examine the excitation energy transfer and quenching pathways in the diatom PSII–FCPII in a greater detail.…”