Research Article

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

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Science  08 Feb 2019:
Vol. 363, Issue 6427, eaav0365
DOI: 10.1126/science.aav0365

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All the hues, even the blues

Photosynthetic organisms must balance maximizing productive light absorption and protecting themselves from too much light, which causes damage. Both tasks require pigments—chlorophylls and carotenoids—which absorb light energy and either transfer it to photosystems or disperse it as heat. Wang et al. determined the structure of a fucoxanthin chlorophyll a/c–binding protein (FCP) from a diatom. The structure reveals the arrangement of the specialized photosynthetic pigments in this light-harvesting protein. Fucoxanthin and chlorophyll c absorb the blue-green light that penetrates to deeper water and is not absorbed well by chlorophylls a or b. FCPs are related to the light-harvesting complexes of plants but have more binding sites for carotenoids and fewer for chlorophylls, which may help transfer and disperse light energy.

Science, this issue p. eaav0365

Structured Abstract

INTRODUCTION

Photosynthetic organisms contain light-harvesting antenna systems to gather light energy required for driving photochemical reactions. Diatoms are a group of eukaryotic algae found in fresh water and oceans throughout the world that help form the basis of ocean primary productivity by fixing massive amounts of carbon dioxide into organic carbon. Diatoms are well adapted to this environment in that they contain light-harvesting antennas with exceptional light harvesting and photoprotection capabilities, called fucoxanthin (Fx) and chlorophyll (Chl) a/c-binding proteins (FCPs). FCPs contain the pigments Chl c and Fx, which enable them to absorb light in the blue-green region that is available under water but not effectively used by organisms that contain exclusively Chl a/b. These pigments also confer on FCPs a robust energy-quenching system necessary to thrive in the surface layer of the ocean, an environment with constantly changing light.

RATIONALE

FCP proteins belong to the superfamily of transmembrane light-harvesting complex (LHC) proteins with low sequence similarity to the main Lhca (LHCI) and Lhcb (LHCII) subunits of the green lineage organisms. The structures of LHCI and LHCII from higher plants, and the structure of LHCI from a red alga, previously revealed the binding sites for pigments in these antenna proteins. This information was not yet known for FCPs, which limited understanding of the mechanism of light absorption in the blue-green region and energy transfer and dissipation.

RESULTS

We solved the x-ray crystal structure of a dimeric FCP from a pennate diatom Phaeodactylum tricornutum at 1.8-Å resolution. The FCP was purified as a dimer, and the structure showed that two monomers are held together by interactions between their transmembrane C helices. This differs from the predominant organization of trimers found in the major LHCII of the green-lineage organisms. Each FCP monomer binds nine Chls and seven Fxs; the number of Chls is much less than the typical 14 Chls, whereas that of Fxs is greater than the three to four carotenoids found in LHCI and LHCII, resulting in a much higher Fx/Chl ratio in FCP than those in LHCI and LHCII. Among the Chls, two are Chl c located at two sides of the transmembrane helices A and B, and they are in close interaction with two nearby Chls a and one Fx, respectively. This indicates fast energy coupling of Chl c not only with Chl a but also with Fx. Each Fx is surrounded by one or more Chls, suggesting efficient energy transfer between them and also efficient dissipation of excess energy under high light conditions through the abundant Fxs. The binding environment of the two end groups of each Fx showed different hydrophilicities within the protein scaffold, suggesting differences in their preferred absorption region of the blue-green light. One diadinoxanthin (Ddx) molecule is assigned to a position close to the monomer-monomer interface because of its weak electron density, suggesting its easy dissociation from the apoprotein and possible involvement in the Ddx-deepoxidation cycle that functions in energy dissipation.

CONCLUSION

The FCP structure revealed a network of Chls a/c and Fxs that enables efficient blue-green light harvesting and energy dissipation in diatoms. The ligand structure and binding environment of each pigment revealed in this study will enable detailed studies on the absorption properties of the individual pigments, energy transfer pathways and dynamics, and excess energy dissipation mechanisms in this group of antennas, by both theoretical calculations and time-resolved spectroscopic approaches.

Structure of a FCP.

The FCP proteins are found in thylakoid membranes of diatoms and related algae and function as light-harvesting antennas in these organisms. They bind, in addition to Chl a commonly present in oxygenic photosynthetic organisms, pigments Chl c and Fx, enabling them to harvest blue-green light, which can penetrate into water more efficiently. The structure reveals close interactions between Chls and Fxs, suggesting efficient energy transfer and dissipation among these pigments.

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.

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