Research Article

Architecture of the photosynthetic complex from a green sulfur bacterium

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Science  20 Nov 2020:
Vol. 370, Issue 6519, eabb6350
DOI: 10.1126/science.abb6350

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Green to the core

Light from the Sun powers most life on today's Earth in some way. The core of the photosynthetic apparatus where charge separation occurs, the reaction center (RC), is thought to have originated a single time and diverged, yielding new kinds of complexes adapted to different tasks and environments. Chen et al. now present an important missing puzzle piece in our understanding of the evolution of RCs: a cryo–electron microscopy structure of the homodimeric type I RC from a green sulfur bacterium bound to a light-harvesting protein. The observed cofactor and pigment arrangement explain biochemical features of this RC and will aid in our understanding of how a single ancestral RC gave rise to the range of structures and functions seen in RCs today.

Science, this issue p. eabb6350

Structured Abstract

INTRODUCTION

Photosynthetic reaction centers (RCs) harvest light energy and convert it into chemical energy, a process that ultimately sustains most life on Earth. RCs are classified as type I (Fe-S type) or type II (quinone type) on the basis of their terminal electron acceptors. Most extant RCs are heterodimers represented by photosystems I and II (PSI and PSII), and they are evolved from homodimeric RCs similar to those seen in green sulfur bacteria (GSB) and heliobacteria. GSB grow in the absence of oxygen, capturing sunlight energy with a light-harvesting structure known as the chlorosome. Fenna-Matthews-Olson proteins (FMO) transfer this energy to a type I RC (GsbRC) to initiate charge-separation and electron-transfer reactions.

RATIONALE

Energy-transfer efficiencies within the chlorosome, from chlorosome to FMO, or within FMO are nearly 100%. However, the efficiency drops to between 35 and 75% for energy transfer from FMO to GsbRC and is substantially lower than the nearly 100% efficiency for transfer from the light-harvesting antenna to the PSI RC in oxygenic photosynthetic organisms. To date, the structures of all typical RCs have been determined except that of the RC from GSB. To reveal the structural characteristics of GsbRC and the basis for the lower energy-transfer efficiency from FMO to GsbRC, we solved the structure of the FMO-GsbRC supercomplex from the GSB Chlorobaculum tepidum at 2.7-Å resolution by cryo–electron microscopy.

RESULTS

The structure contains one FMO trimer attached at a distal end of the homodimeric GsbRC, and the edge-to-edge distance between the bacteriochlorophylls of FMO and GsbRC is >21 Å. This distance is considerably longer than that seen in other photosynthetic systems and thus explains the reduced efficiency of energy transfer between these two complexes. The GsbRC binds 26 bacteriochlorophylls a and 4 chlorophylls a, among which the chlorophylls a are assigned to the first and second electron acceptors in the electron-transfer chain. No quinones were found between the secondary electron acceptor A0 and the Fe-S cluster, and the arrangement of the chlorophylls in the two branches of the electron-transfer chain is approximately symmetric at the current resolution. The total number of (bacterio)chlorophylls, 30, is substantially less than the 60 (bacterio)chlorophylls in the heliobacterial RC and the 87 chlorophylls in the PSI core but is close to the 35 chlorophylls in the PSII core. The 30 (bacterio)chlorophylls in our structure are located at conserved positions relative to those of other RCs and are arranged into two layers, representing common features of both type I and II RCs. We observed a carotenoid derivative between the two layers (instead of linker chlorophylls seen in other RCs); this may represent an ancestral feature of RCs. In each layer, chlorophylls are clustered into two separated groups, similar to the arrangement of the PSII core but in contrast to that of other type I RCs.

CONCLUSION

The structure of the GsbRC explains the imperfect efficiency of energy transfer from FMO to GsbRC and reveals a number of features that may represent an ancestral form of both type I and II RCs. These features include a homodimeric core with fewer pigments associated, a conserved core protein structure, distinctive pigment arrangement similar to that seen in PSII instead of PSI, and a chlorobactene derivative located between the two chlorophyll layers within the membrane. With this structure, we now have a complete set of structures from different groups of photosynthetic organisms, allowing us to examine the evolution of photosystems in greater detail. By revealing the arrangement of proteins and pigments, including features of both type I and II RCs, the structure provides valuable insight into how extant members of this family of proteins diverged from a common RC ancestor.

Photosynthetic apparatus of GSB and atomic structure of the FMO-RC complex.

GSB perform photosynthesis by using light energy to transform substrates of carbon dioxide and hydrogen sulfide to organic compounds, water, and sulfur. One unit of the photosynthetic apparatus in GSB contains a peripheral antenna chlorosome, light-harvesting FMO, and a membrane-embedded RC. The energy absorbed by the chlorosome is transferred through FMO to the RC to initiate charge-separation and electron-transfer reactions. The overall structure and cofactor arrangements in this supercomplex help explain rates of energy transfer and the evolution of features observed in oxygenic photosystems. h, Planck’s constant; ν, photon frequency.

Abstract

The photosynthetic apparatus of green sulfur bacteria (GSB) contains a peripheral antenna chlorosome, light-harvesting Fenna-Matthews-Olson proteins (FMO), and a reaction center (GsbRC). We used cryo–electron microscopy to determine a 2.7-angstrom structure of the FMO-GsbRC supercomplex from Chlorobaculum tepidum. The GsbRC binds considerably fewer (bacterio)chlorophylls [(B)Chls] than other known type I RCs do, and the organization of (B)Chls is similar to that in photosystem II. Two BChl layers in GsbRC are not connected by Chls, as seen in other RCs, but associate with two carotenoid derivatives. Relatively long distances of 22 to 33 angstroms were observed between BChls of FMO and GsbRC, consistent with the inefficient energy transfer between these entities. The structure contains common features of both type I and type II RCs and provides insight into the evolution of photosynthetic RCs.

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