Research Article

The pigment-protein network of a diatom photosystem II–light-harvesting antenna supercomplex

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Science  02 Aug 2019:
Vol. 365, Issue 6452, eaax4406
DOI: 10.1126/science.aax4406

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A light-harvesting array in diatoms

Photosynthetic organisms use huge arrays of pigments to draw light energy into the core of photosystem II. The arrangement of these pigments influences how much energy reaches the reaction center. Pi et al. determined the structure of photosystem II from a diatom in complex with an antenna of fucoxanthin–chlorophyll a/c binding proteins (FCPs) (see the Perspective by Büchel). The specialized pigments in this complex allow microalgae to harvest light within a wide range of the visible spectrum. The FCPs are arranged in a pattern analogous to light-harvesting complexes in plants.

Science, this issue p. eaax4406; see also p. 447

Structured Abstract

INTRODUCTION

Photosystem II (PSII) is a pigment-protein complex and catalyzes light-induced water splitting in photosynthesis, converting light energy from the Sun into chemical energy and providing molecular oxygen to the atmosphere. To make full use of light energy, photosynthetic organisms have developed light-harvesting complexes (LHCs) to gather light energy and transfer it to photosynthetic reaction centers. Many LHCII subunits are associated with a core PSII, forming PSII-LHCII supercomplexes. LHC proteins vary across lineages of photosynthetic organisms and enable groups of organisms to cope with different light environments. In addition to light-harvesting, LHCs also have a role in dissipation of excess energy under strong light illumination so as to avoid damage to photosystems caused by intense light.

RATIONALE

LHCIIs of green-lineage photosynthetic organisms bind chlorophyll (Chl) a/b as their main pigments, whereas some organisms of the red lineage bind Chl a/c as their main pigments. Diatoms are one of the main groups in the red lineage and contribute ~20% of all primary productivity on Earth. The light-harvesting antennas of diatoms are known as Chl a/c and fucoxanthin (Fx) binding proteins, or FCPs, and enable diatoms to efficiently use blue-green light available under water. The distinct pigment composition and organization of the PSII-FCPII supercomplex confers on diatoms the capacity to efficiently dissipate excess energy when necessary. A structure of PSII-FCPII of diatoms greatly expands our understanding of the energy harvesting and dissipation mechanisms in a dominant photosynthetic organism.

RESULTS

We used single-particle cryo–electron microscopy analysis to elucidate a structure of the PSII-FCPII supercomplex from the diatom Chaetoceros gracilis at a resolution of 3.0 Å. The supercomplex contains two protomers with 24 subunits in the PSII core and 11 subunits in FCPII, giving rise to a total of 70 subunits with an overall molecular weight of 1.4 MDa. The PSII core is largely similar to that of cyanobacteria and higher plants, but we found five extrinsic proteins that play a role in the oxygen-evolving reaction. Two additional transmembrane subunits located at the periphery of the PSII core help to connect the PSII core with the FCPII subunits. The major FCPII is organized into two tetramers: one is tightly associated whereas the other is moderately associated with the PSII core. In addition, three FCP monomers are associated with each PSII core; among them, two connect the moderately associated FCPII tetramer with the PSII core whereas one is associated at the periphery of the moderately associated FCPII tetramer. These arrangements differ from those found in the PSII-LHCII supercomplexes of the green-lineage organisms, and the locations of the tightly and moderately associated FCP tetramers are opposite to those of the strongly and moderately associated trimers found in PSII-LHCII. On the other hand, locations of the two monomeric FCPs (FCP-D and FCP-E) resemble those of CP24 and CP29 in higher-plant PSII-LHCIIs in that both of them connect the moderately associated FCP tetramer or LHCII trimer with the PSII core.

CONCLUSION

Our PSII-FCPII structure reveals the arrangement of a huge number of pigments (Chls a/c and Fxs) that contribute to energy transfer and dissipation in this supercomplex. Theoretical and time-resolved spectroscopic studies can be designed on the basis of this structure and, in combination with reexamination of existing results, will reveal more details of these reactions. The diatom PSII core also contains transmembrane and extrinsic subunits that may provide clues to changes occuring in the PSII core during evolution.

Model of a diatom PSII-FCPII supercomplex embedded in the thylakoid membrane.

The PSII-FCPII supercomplex contains 35 protein subunits and a number of pigments and cofactors and catalyzes light-induced electron transfer and water-splitting reactions. The latter occur in the lumen of the thylakoid membrane, leading to the generation of protons and molecular oxygen. Light is absorbed by the light-harvesting antenna pigments, among which Chl c and Fx enable absorption of blue-green light available under water. In addition, diadinoxanthin associated with FCPII plays important roles in photoprotection.

Abstract

Diatoms play important roles in global primary productivity and biogeochemical cycling of carbon, in part owing to the ability of their photosynthetic apparatus to adapt to rapidly changing light intensity. We report a cryo–electron microscopy structure of the photosystem II (PSII)–fucoxanthin (Fx) chlorophyll (Chl) a/c binding protein (FCPII) supercomplex from the centric diatom Chaetoceros gracilis. The supercomplex comprises two protomers, each with two tetrameric and three monomeric FCPIIs around a PSII core that contains five extrinsic oxygen-evolving proteins at the lumenal surface. The structure reveals the arrangement of a huge pigment network that contributes to efficient light energy harvesting, transfer, and dissipation processes in the diatoms.

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