Anaerobic energy dissipation by glycosylated carotenoids in the green sulfur bacterium Chlorobaculum tepidum

Azai, Chihiro; Harada, Jiro; Fujimoto, Shogo; Masuda, Shinji; Kosumi, Daisuke

doi:10.1016/j.jphotochem.2020.112828

Cited by 6 publications

(5 citation statements)

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“…F39 is a glycosylated carotenoid that is bound only to the GsbRC core (Takaichi and Oh-oka 1999 ) in a region that shows structural conservation with PSII as noted above. A GsbRC mutant lacking carotenoid glycosylation shows growth defects under high light and slower quenching of the core antenna BChl a fluorescence (Azai et al 2020 ); therefore, the F39 in the GsbRC must be responsible for this mutant phenotype, quenching excitation energy of BChl 808 via BChl 805. Though green sulfur bacteria typically reside in anaerobic environments, it is clear that mechanisms are present for coping with at least low levels of oxygen.…”

Section: Comparison Of the Gsbrc To Other Rcsmentioning

confidence: 99%

Recent advances in the structural diversity of reaction centers

2021

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Photosynthetic reaction centers (RC) catalyze the conversion of light to chemical energy that supports life on Earth, but they exhibit substantial diversity among different phyla. This is exemplified in a recent structure of the RC from an anoxygenic green sulfur bacterium (GsbRC) which has characteristics that may challenge the canonical view of RC classification. The GsbRC structure is analyzed and compared with other RCs, and the observations reveal important but unstudied research directions that are vital for disentangling RC evolution and diversity. Namely, (1) common themes of electron donation implicate a Ca2+ site whose role is unknown; (2) a previously unidentified lipid molecule with unclear functional significance is involved in the axial ligation of a cofactor in the electron transfer chain; (3) the GsbRC features surprising structural similarities with the distantly-related photosystem II; and (4) a structural basis for energy quenching in the GsbRC can be gleaned that exemplifies the importance of how exposure to oxygen has shaped the evolution of RCs. The analysis highlights these novel avenues of research that are critical for revealing evolutionary relationships that underpin the great diversity observed in extant RCs.

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Section: Comparison Of the Gsbrc To Other Rcsmentioning

confidence: 99%

Recent advances in the structural diversity of reaction centers

2021

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“…11c ). These interactions provide a highly hydrophobic environment for stabilizing F39 binding 62 . On the opposite side of the PscA dimer, partly because of the lower occupancy of PscC, F39 does not bind strongly to PscA2, and its density is not seen in our cryo-EM map.…”

Section: Resultsmentioning

confidence: 99%

Molecular asymmetry of a photosynthetic supercomplex from green sulfur bacteria

et al. 2022

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The photochemical reaction center (RC) features a dimeric architecture for charge separation across the membrane. In green sulfur bacteria (GSB), the trimeric Fenna-Matthews-Olson (FMO) complex mediates the transfer of light energy from the chlorosome antenna complex to the RC. Here we determine the structure of the photosynthetic supercomplex from the GSB Chlorobaculum tepidum using single-particle cryogenic electron microscopy (cryo-EM) and identify the cytochrome c subunit (PscC), two accessory protein subunits (PscE and PscF), a second FMO trimeric complex, and a linker pigment between FMO and the RC core. The protein subunits that are assembled with the symmetric RC core generate an asymmetric photosynthetic supercomplex. One linker bacteriochlorophyll (BChl) is located in one of the two FMO-PscA interfaces, leading to differential efficiencies of the two energy transfer branches. The two FMO trimeric complexes establish two different binding interfaces with the RC cytoplasmic surface, driven by the associated accessory subunits. This structure of the GSB photosynthetic supercomplex provides mechanistic insight into the light excitation energy transfer routes and a possible evolutionary transition intermediate of the bacterial photosynthetic supercomplex from the primitive homodimeric RC.

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“…The GSB RC-PS associated chlorobactene carotenoid designated as F26, bound in a position adjacent to the core complex interface with FMO [ 5 ], was shown to be involved in both energy quenching and transfer processes [ 66 ]. Accordingly, a slowing of fluorescence quenching of the core LH-BChls was demonstrated in a Cba.…”

Section: Further Insights Into the Evolutionary Origins Of Oxygenic P...mentioning

confidence: 99%

“…This runs counter to the earlier but largely unsupported views that anoxygenic Type II RCs are more ancient than the Type II RCs of their oxygenic counterparts [ 70 ] and that the anoxygenic to oxygenic photosynthetic transition occurred when a PSI containing cyanobacterium formed PSII with the ability to oxidize H 2 O (summarized by Olson and Blankenship [ 71 ]). Instead, the early origins of both PSI and II are now supported by a considerable body of evidence [ 2 , 12 , 13 , 64 , 65 , 66 , 67 , 68 , 69 , 72 , 73 ] forming the basis for the proposal that the gene duplication event, resulting in the heterodimerization of a homodimeric ancestor of PSII into distinct D1 and D2 polypeptides likely predated the subsequent evolution of the well-described L and M polypeptides of anoxygenic Type II RC [ 69 , 71 ].…”

Section: Further Insights Into the Evolutionary Origins Of Oxygenic P...mentioning

confidence: 99%

What We Are Learning from the Diverse Structures of the Homodimeric Type I Reaction Center-Photosystems of Anoxygenic Phototropic Bacteria

Niederman

2024

Biomolecules

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A Type I reaction center (RC) (Fe-S type, ferredoxin reducing) is found in several phyla containing anoxygenic phototrophic bacteria. These include the heliobacteria (HB), the green sulfur bacteria (GSB), and the chloracidobacteria (CB), for which high-resolution homodimeric RC-photosystem (PS) structures have recently appeared. The 2.2-Å X-ray structure of the RC-PS of Heliomicrobium modesticaldum revealed that the core PshA apoprotein (PshA-1 and PshA-2 homodimeric pair) exhibits a structurally conserved PSI arrangement comprising five C-terminal transmembrane α-helices (TMHs) forming the RC domain and six N-terminal TMHs coordinating the light-harvesting (LH) pigments. The Hmi. modesticaldum structure lacked quinone (Q) molecules, indicating that electrons were transferred directly from the A0 (81-OH-chlorophyll (Chl) a) acceptor to the FX [4Fe-4S] component, serving as the terminal RC acceptor. A pair of additional TMHs designated as Psh X were also found that function as a low-energy antenna. The 2.5-Å resolution cryo-electron microscopy (cryo-EM) structure for the RC-PS of the green sulfur bacterium Chlorobaculum tepidum included a pair of Fenna–Matthews–Olson protein (FMO) antennae, which transfer excitations from the chlorosomes to the RC-PS (PscA-1 and PscA-2) core. A pair of cytochromes cZ (PscC) molecules was also revealed, acting as electron donors to the RC bacteriochlorophyll (BChl) a’ special pair, as well as PscB, housing the [4Fe-4S] cluster FA and FB, and the associated PscD protein. While the FMO components were missing from the 2.6-Å cryo-EM structure of the Zn- (BChl) a’ special pair containing RC-PS of Chloracidobacterium thermophilum, a unique architecture was revealed that besides the (PscA)2 core, consisted of seven additional subunits including PscZ in place of PscD, the PscX and PscY cytochrome c serial electron donors and four low mol. wt. subunits of unknown function. Overall, these diverse structures have revealed that (i) the HB RC-PS is the simplest light–energy transducing complex yet isolated and represents the closest known homolog to a common homodimeric RC-PS ancestor; (ii) the symmetrically localized Ca2+-binding sites found in each of the Type I homodimeric RC-PS structures likely gave rise to the analogously positioned Mn4CaO5 cluster of the PSII RC and the TyrZ RC donor site; (iii) a close relationship between the GSB RC-PS and the PSII Chl proteins (CP)43 and CP47 was demonstrated by their strongly conserved LH-(B)Chl localizations; (iv) LH-BChls of the GSB-RC-PS are also localized in the conserved RC-associated positions of the PSII ChlZ-D1 and ChlZ-D2 sites; (v) glycosylated carotenoids of the GSB RC-PS are located in the homologous carotenoid-containing positions of PSII, reflecting an O2-tolerance mechanism capable of sustaining early stages in the evolution of oxygenic photosynthesis. In addition to the close relationships found between the homodimeric RC-PS and PSII, duplication of the gene encoding the ancestral Type I RC apoprotein, followed by genetic divergence, may well account for the appearance of the heterodimeric Type I and Type II RCs of the extant oxygenic phototrophs. Accordingly, the long-held view that PSII arose from the anoxygenic Type II RC is now found to be contrary to the new evidence provided by Type I RC-PS homodimer structures, indicating that the evolutionary origins of anoxygenic Type II RCs, along with their distinct antenna rings are likely to have been preceded by the events that gave rise to their oxygenic counterparts.

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Anaerobic energy dissipation by glycosylated carotenoids in the green sulfur bacterium Chlorobaculum tepidum

Cited by 6 publications

References 48 publications

Recent advances in the structural diversity of reaction centers

Recent advances in the structural diversity of reaction centers

Molecular asymmetry of a photosynthetic supercomplex from green sulfur bacteria

What We Are Learning from the Diverse Structures of the Homodimeric Type I Reaction Center-Photosystems of Anoxygenic Phototropic Bacteria

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