Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC–LH1 supercomplex

Bracun, Laura; Yamagata, Atsushi; Christianson, Bern M.; Negami, Tatsuki; Zou, Baohua; Terada, Tohru; Canniffe, Daniel P.; Shirouzu, Mikako; Li, Mei; Liu, Luning

doi:10.1038/s41467-022-29563-3

Cited by 38 publications

(72 citation statements)

References 91 publications

(109 reference statements)

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“…globiformis . On the other hand, PufX is located on one edge of the open-shaped LH1 ring 18 – 23 . Occupation of this position by PufX prevents LH1 from forming a closed ring.…”

Section: Discussionmentioning

confidence: 99%

“…Instead, these species use both a soluble Cyt c 2 17 and a membrane-anchored mono-heme Cyt c y 4 to facilitate electron transfer to the RC. In all Rhodobacter species, there is a unique protein in the light-harvesting 1–reaction center (LH1–RC) complex called PufX that interacts with the RC-L subunit and LH1 polypeptides 18 – 23 . PufX (encoded by the gene pufX 24 , 25 ) is a transmembrane protein composed of about 80 amino acids, and pufX is located at the same position as pufC —immediately following pufM (the gene encoding the RC-M subunit) in the puf operon.…”

Section: Introductionmentioning

confidence: 99%

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An LH1–RC photocomplex from an extremophilic phototroph provides insight into origins of two photosynthesis proteins

et al. 2022

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Rhodopila globiformis is the most acidophilic of anaerobic purple phototrophs, growing optimally in culture at pH 5. Here we present a cryo-EM structure of the light-harvesting 1–reaction center (LH1–RC) complex from Rhodopila globiformis at 2.24 Å resolution. All purple bacterial cytochrome (Cyt, encoded by the gene pufC) subunit-associated RCs with known structures have their N-termini truncated. By contrast, the Rhodopila globiformis RC contains a full-length tetra-heme Cyt with its N-terminus embedded in the membrane forming an α-helix as the membrane anchor. Comparison of the N-terminal regions of the Cyt with PufX polypeptides widely distributed in Rhodobacter species reveals significant structural similarities, supporting a longstanding hypothesis that PufX is phylogenetically related to the N-terminus of the RC-bound Cyt subunit and that a common ancestor of phototrophic Proteobacteria contained a full-length tetra-heme Cyt subunit that evolved independently through partial deletions of its pufC gene. Eleven copies of a novel γ-like polypeptide were also identified in the bacteriochlorophyll a-containing Rhodopila globiformis LH1 complex; γ-polypeptides have previously been found only in the LH1 of bacteriochlorophyll b-containing species. These features are discussed in relation to their predicted functions of stabilizing the LH1 structure and regulating quinone transport under the warm acidic conditions.

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“…globiformis . On the other hand, PufX is located on one edge of the open-shaped LH1 ring 18 – 23 . Occupation of this position by PufX prevents LH1 from forming a closed ring.…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

An LH1–RC photocomplex from an extremophilic phototroph provides insight into origins of two photosynthesis proteins

et al. 2022

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“…Compared to the LH that contains different compositional and structural features, the core components of the RC, including the L, M-subunits and cofactors are structurally conserved with that of purple bacteria ( Supplementary Figures 1A–D , 2A,B ). Notably, purple bacteria usually contain an H subunit that is important for regulating the assembly and electron transfer of the RC ( Debus et al, 1985 ; Sun et al, 2015 ; Sun, 2017 ; Cao et al, 2022 ). However, presence of the H subunit often increased the distance between Q-side of the RC and the electrode, and decreased the electron transfer efficiency in PBECs.…”

Section: Discussion and Future Perspectivementioning

confidence: 99%

Preparation of Photo-Bioelectrochemical Cells With the RC-LH Complex From Roseiflexus castenholzii

Xin²,

Liu³

et al. 2022

Front. Microbiol.

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Roseiflexus castenholzii is an ancient green non-sulfur bacteria that absorbs the solar energy through bacteriochlorophylls (BChls) bound in the only light harvesting (LH) complex, and transfers to the reaction center (RC), wherein primary charge separation occurs and transforms the energy into electrochemical potentials. In contrast to purple bacteria, R. castenholzii RC-LH (rcRC-LH) does not contain an H subunit. Instead, a tightly bound tetraheme cytochrome c subunit is exposed on the P-side of the RC, which contains three BChls, three bacteriopheophytins (BPheos), two menaquinones, and one iron for electron transfer. These novel structural features of the rcRC-LH are advantageous for enhancing the electron transfer efficiency and subsequent photo-oxidation of the c-type hemes. However, the photochemical properties of rcRC-LH and its applications in developing the photo-bioelectrochemical cells (PBECs) have not been characterized. Here, we prepared a PBEC using overlapped fluorine-doped tin oxide (FTO) glass and Pt-coated glass as electrodes, and rcRC-LH mixed with varying mediators as the electrolyte. Absence of the H subunit allows rcRC-LH to be selectively adhered onto the hydrophilic surface of the front electrode with its Q-side. Upon illumination, the photogenerated electrons directly enter the front electrode and transfer to the counter electrode, wherein the accepted electrons pass through the exposed c-type hemes to reduce the excited P+, generating a steady-state current of up to 320 nA/cm2 when using 1-Methoxy-5-methylphenazinium methyl sulfate (PMS) as mediator. This study demonstrated the novel photoelectric properties of rcRC-LH and its advantages in preparing effective PBECs, showcasing a potential of this complex in developing new type PBECs.

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“…This stabilising effect may be analogous to the role that PufX plays in the primarily dimeric Rhodobacter sphaeroides RC–LH1 [50]. Deletion of the pufX gene leads to formation of solely monomeric RC–LH1, and the recent cryo-EM structure of this complex was solved at much lower resolution than the PufX-containing dimer or monomer, attributed to PufX’s role in orienting the RC within LH1 [50,18]. It is interesting that we do not observe assembly of RCs without LH1 in the WT under either white light or halogen light conditions.…”

Section: Discussionmentioning

confidence: 99%

“…Some LH1 antennas also contain additional subunits; the Rhodopseudomonas palustris LH1 ring contains a single transmembrane helix known as protein W [11,12], LH1 from Rhodobacter spp. contains a PufX polypeptide [13][14][15], and a further subgroup of these organisms additionally contain PufY [16][17][18]. These polypeptides create a channel in the LH1 ring allowing quinone/quinol exchange between the RC and the cytochrome bc1 complex [19,20].…”

Section: Introductionmentioning

confidence: 99%

The role of the γ subunit in the photosystem of the lowest-energy phototrophs

Namoon

Rudling

Canniffe

2022

Preprint

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Purple phototrophic bacteria use a core "photosystem" consisting of light harvesting antenna complex 1 (LH1) surrounding the reaction centre (RC), which primarily absorbs far-red/near-infrared light and converts it to chemical energy. Species in the Blastochloris genus, which are able to use light >1000nm for photosynthesis, use bacteriochlorophyll (BChl) b rather than the more common BChl a as their major photopigment, and also uniquely assemble LH1 with an additional polypeptide subunit, LH1γ, encoded by multiple open reading frames in their genomes. In order to assign a role to this subunit, we deleted the four LH1γ-encoding genes in the model Blastochloris viridis. Interestingly, growth under halogen bulbs routinely used for cultivation of anoxygenic phototrophs yielded cells displaying an absorption maximum of 825 nm, similar to that of the RC complex without LH1, but growth under white light from fluorescent bulbs yielded cells with an absorption maximum at 972 nm. HPLC analysis of pigment composition and sucrose density gradient fractionation demonstrate that the mutant grown in white light assembles RC-LH1, albeit with an absorption maximum blue-shifted by 46 nm relative to the WT complex. Wavelengths between 900-1000 nm transmit poorly through the atmosphere due to strong absorption by water, thus our results provide an evolutionary rationale for the incorporation of the γ subunit into the LH1 ring; this polypeptide red-shifts the absorption maximum of the complex to a range of the spectrum where the photons are of lower energy but are more abundant. Finally, we transformed the mutant with plasmids carrying genes encoding natural LH1γ variants and demonstrate that the polypeptide found in the WT complex red-shifts absorption back to 1018 nm, but incorporation of a distantly-related variant results in only a moderate red-shift. This result suggests that tuning the absorption maximum of this organism is possible, and may permit light capture past the current low-energy limit of natural photosynthesis.

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Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC–LH1 supercomplex

Cited by 38 publications

References 91 publications

An LH1–RC photocomplex from an extremophilic phototroph provides insight into origins of two photosynthesis proteins

An LH1–RC photocomplex from an extremophilic phototroph provides insight into origins of two photosynthesis proteins

Preparation of Photo-Bioelectrochemical Cells With the RC-LH Complex From Roseiflexus castenholzii

The role of the γ subunit in the photosystem of the lowest-energy phototrophs

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