Review Article

Atomic structure of the photosynthetic reaction center from a green sulfur bacterium

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  • ①Center of Cryo-Electron Microscopy, Sir Run Run Shaw Hospital, Department of Biophysics, School of Medicine, Zhejiang University, Hangzhou 310058, China; ②Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

Received date: 2021-03-05

  Online published: 2021-06-13

Abstract

Green sulfur bacteria are strictly anaerobic photosynthetic bacteria, and perform anoxygenic photosynthesis by obtaining electrons from sulfides. The photosynthetic light-reaction system of green sulfur bacteria consists of a peripheral light-harvesting antenna called chlorosome, an energy transmitter FMO protein and the reaction center complex. In this paper, we describe the atomic structure of the FMO-reaction center complex from a green sulfur bacterium solved by cryo-electron microscopy, insight into the energy transfer mechanism within the complex based on the structure obtained, and their implications on the evolution of early photoreaction systems.

Cite this article

CHEN Jinghua, KUANG Tingyun, SHEN Jianren, ZHANG Xing . Atomic structure of the photosynthetic reaction center from a green sulfur bacterium[J]. Chinese Journal of Nature, 2021 , 43(3) : 189 -198 . DOI: 10.3969/j.issn.0253-9608.2021.03.004

References

[1] ALLEN J P, WILLIAMS J C. Photosynthetic reaction centers [J].  FEBS Letters, 1998, 438: 5-9.

[2] CARDONA T. A fresh look at the evolution and diversification of photochemical reaction centers [J]. Photosynthesis Research, 2015, 126: 111-134. 

[3] DEISENHOFER J, EPP O, MIKI K, et al. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution [J]. Nature, 1985, 318: 618-624. [4] KARRASCH S, BULLOUGH P A, GHOSH R. The 8.5 Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits [J]. The EMBO Journal, 1995, 14: 631-638. 

[5] ALEKSANDER W R, TINA D H, JUNE S, et al. Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris [J]. Science, 2003, 302: 1969-1972. 

[6] QIAN P, PAPIZ M Z, JACKSON P J, et al. Three-dimensional structure of the Rhodobacter sphaeroides RC-LH1-PufX complex: dimerization and quinone channels promoted by PufX [J]. Biochemistry, 2013, 52: 7575-7585. 

[7] JORDAN P, FROMME P, WITT H T, et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution [J]. Nature, 2001, 411: 909-917. 

[8] UMENA Y, KAWAKAMI K, SHEN J R, et al. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å [J]. Nature, 2011, 473: 55-60. 

[9] NIWA S, YU L J, TAKEDA K, et al. Structure of the LH1-RC complex from Thermochromatium tepidum at 3.0 Å [J]. Nature, 2014, 508: 228-232. 

[10] GISRIEL C, SARROU I, FERLEZ B, et al. Structure of a symmetric photosynthetic reaction center–photosystem [J]. Science, 2017, 357: 1021-1025. 

[11] YU L J, SUGA M, WANG-OTOMO Z Y, et al. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution [J]. Nature, 2018, 556: 209-213. 

[12] XIN Y Y, SHI Y, NIU T, et al. Cryo-EM structure of the RC-LH core complex from an early branching photosynthetic prokaryote [J]. Nature Communications, 2018, 9: 1568. DOI: 10.1038/s41467-018- 03881-x. 

[13] QIAN P, SIEBERT C A, WANG P, et al. Cryo-EM structure of the Blastochloris viridis LH1-RC complex at 2.9 Å [J]. Nature, 2018, 556: 203-208. 

[14] CARDONA T, RUTHERFORD A W. Evolution of photochemical reaction centres: more twists [J]. Trends in Plant Science, 2019, 24: 1008-1021. 

[15] CARDONA T. Thinking twice about the evolution of photosynthesis [J]. Open Biology, 2019, 9(9): 180246. DOI: 10.1098/rsob.180246. 

[16] OLSON J M, BLANKENSHIP R E. Thinking about the evolution of photosynthesis [J]. Photosynthesis Research, 2004, 80: 373-386. 

[17] HE Z, FERLEZ B, KURASHOV V, et al. Reaction centers of the thermophilic microaerophile, Chloracidobacterium thermophilum (Acidobacteria) I: biochemical and biophysical characterization [J]. Photosynthesis Research, 2019, 142: 87-103. 

[18] BEATTY J T, OVERMANN J, LINCE M T, et al. An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent [J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102: 9306-9310. 

[19] IMHOFF J F. The family chlorobiaceae [M]//ROSENBERG E, DELONG E F, LORY S, et al(eds). The Prokaryotes. Berlin: Springer, 2014. DOI: 10.1007/978-3-642-38954-2_142. 

[20] 翁羽翔. 光合细菌分子自组装捕光天线相干激子态传能机制的人工模拟[J]. 物理, 2016, 45(12): 798-800. DOI: 10.7693/ wl20161207. 

[21] WAHLUND T M, WOESE C R, CASTENHOLZ R W, et al. A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov [J]. Archives of Microbiology, 1991, 156: 81-90. 

[22] PEDERSEN M Ø, UNDERHAUG J, DITTMER J, et al. The threedimensional structure of CsmA: a small antenna protein from the green sulfur bacterium Chlorobium tepidum [J]. FEBS Letters, 2008, 582: 2869-2874. 

[23] HOHMANN-MARRIOTT M F, BLANKENSHIP R E, ROBERSON R W. The ultrastructure of Chlorobium tepidum chlorosomes revealed by electron microscopy [J]. Photosynthesis Research, 2005, 86: 145-154. 

[24] ORF G S, BLANKENSHIP R E. Chlorosome antenna complexes from green photosynthetic bacteria [J]. Photosynthesis Research, 2013, 116: 315-331. 

[25] NOZAWA T, OHTOMO K, SUZUKI M, et al. Structures of chlorosomes and aggregated BChlc in Chlorobium tepidum from solid state high resolution CP/MAS13C NMR [J]. Photosynthesis Research, 1994, 41: 211-223. 

[26] OOSTERGETEL G T, VAN AMERONGEN H, BOEKEMA E J. The chlorosome: a prototype for efficient light harvesting in photosynthesis [J]. Photosynthesis Research, 2010, 104: 245-255. 

[27] NIELSEN J T, KULMINSKAYA N V, BJERRING M, et al. In situ high-resolution structure of the baseplate antenna complex in Chlorobaculum tepidum [J]. Nature Communications, 2016, 7: 12454. DOI: 10.1038/ncomms12454. 

[28] FENNA R E, MATTHEWS B W. Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola [J]. Nature, 1975, 258: 573-577. 

[29] OLSON J M. The FMO protein [J]. Photosynthesis Research, 2004, 80: 181-187. 

[30] CAMARA-ARTIGAS A, BLANKENSHIP R E, ALLEN J P. The structure of the FMO protein from Chlorobium tepidum at 2.2 Å resolution [J]. Photosynthesis Research, 2003, 75: 49-55. 

[31] LARSON C R, SENG C O, LAUMAN L, et al. The threedimensional structure of the FMO protein from Pelodictyon phaeum and the implications for energy transfer [J]. Photosynthesis Research, 2011, 107: 139-150. 

[32] KELL A, ACHARYA K, ZAZUBOVICH V, et al. On the controversial nature of the 825 nm exciton band in the FMO protein complex [J]. The Journal of Physical Chemistry Letters, 2014, 5: 1450-1456. 

[33] KELL A, KHMELNITSKIY A Y, REINOT T, et al. On uncorrelated inter-monomer Forster energy transfer in Fenna-Matthews-Olson complexes [J]. Journal of the Royal Society Interface, 2019, 16: 20180882. DOI: 10.1098/rsif.2018.0882. 

[34] HAUSKA G, SCHOEDL T, REMIGY H, et al. The reaction center of green sulfur bacteria [J]. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2001, 1507: 260-277. 

[35] EISEN J A, NELSON K E, PAULSEN I T, et al. The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium [J]. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99: 9509-9514. 

[36] BUTTNER M, XIE D L, NELSON H, et al. The photosystem I-like P840-reaction center of green S-bacteria is a homodimer [J]. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1992, 1101: 154-156. 

[37] BUTTNER M, XIE D L, NELSON H, et al. Photosynthetic reaction center genes in green sulfur bacteria and in photosystem I are related [J]. Proceedings of the National Academy of Sciences of the United States of America, 1992, 89: 8135-8139. 

[38] TSUKATANI Y, MIYAMOTO R, ITOH S, et al. Function of a PscD subunit in a homodimeric reaction center complex of the photosynthetic green sulfur bacterium Chlorobium tepidum studied by insertional gene inactivation. Regulation of energy transfer and ferredoxin-mediated NADP+ reduction on the cytoplasmic side [J]. Journal of Biological Chemistry, 2004, 279: 51122-51130.

[39] HIRANO Y, HIGUCHI M, AZAI C, et al. Crystal structure of the electron carrier domain of the reaction center cytochrome c(z) subunit from green photosynthetic bacterium Chlorobium tepidum [J]. Journal of Molecular Biology, 2010, 397: 1175-1187. 

[40] PERMENTIER H P, SCHMIDT K A, KOBAYASHI M, et al. Composition and optical properties of reaction centre core complexes from the green sulfur bacteria Prosthecochloris aestuarii and Chlorobium tepidum [J]. Photosynthesis Research, 2000, 64: 27-39.

[41] GRIESBECK C, HAGER-BRAUN C, ROGL H, et al. Quantitation of P840 reaction center preparations from Chlorobium tepidum: chlorophylls and FMO-protein [J]. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1998, 1365: 285-293. 

[42] KOBAYASHI M, OH-OKA H, AKUTSU S, et al. The primary electron acceptor of green sulfur bacteria, bacteriochlorophyll 663, is chlorophyll a esterified with ∆2,6-phytadienol [J]. Photosynthesis Research, 2000, 63: 269-280. 

[43] TSIOTIS G, HAGER-BRAUN C, WOLPENSINGER B, et al. Structural analysis of the photosynthetic reaction center from the green sulfur bacterium Chlorobium tepidum [J]. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1997, 1322: 163-172. 

[44] REMIGY H W, STAHLBERG H, FOTIADIS D, et al. The reaction center complex from the green sulfur bacterium Chlorobium tepidum: a structural analysis by scanning transmission electron microscopy [J]. Journal of Molecular Biology, 1999, 290: 851-858.

 [45] BÍNA D, GARDIAN Z, VÁCHA F, et al. Native FMO-reaction center supercomplex in green sulfur bacteria: an electron microscopy study [J]. Photosynthesis Research, 2016, 128: 93-102. 

[46] CHEN J H, WU H, XU C, et al. Architecture of the photosynthetic complex from a green sulfur bacterium [J]. Science, 2020, 370(6519): eabb6350. DOI: 10.1126/science.abb6350. 

[47] HAGER-BRAUN C, XIE D L, JAROSCH U, et al. Stable photobleaching of P840 in Chlorobium reaction center preparations: Presence of the 42-kDa bacteriochlorophyll a protein and a 17-kDa polypeptide [J]. Biochemistry, 1995, 34: 9617-9624. 

[48] CAUSGROVE T P, BRUNE D C, WANG J, et al. Energy transfer kinetics in whole cells and isolated chlorosomes of green photosynthetic bacteria [J]. Photosynthesis Research, 1990, 26: 39-48. 

[49] FETISOVA Z, FREIBERG A, TIMPMANN K. Long-range molecular order as an efficient strategy for light harvesting in photosynthesis [J]. Nature, 1988, 334: 633-634. 

[50] FRANCKE C, OTTE S C M, MILLER M, et al. Energy transfer from carotenoid and FMO-protein in subcellular preparations from green sulfur bacteria. Spectroscopic characterization of an FMOreaction center core complex at low temperature [J]. Photosynthesis Research, 1996, 50: 71-77. 

[51] NELSON N. Plant photosystem I—The most efficient nanophotochemical machine [J]. Journal of Nanoscience and Nanotechnology, 2009, 9: 1709-1713. 

[52] HE G, NIEDZWIEDZKI D M, ORF G S, et al. Dynamics of energyand electron transfer in the FMO-reaction center core complex from the phototrophic green sulfur bacterium chlorobaculum tepidum [J]. The Journal of Physical Chemistry B, 2015, 119: 8321-8329. 

[53] MAGDAONG N C M, NIEDZWIEDZKI D M, SAER R G, et al. Excitation energy transfer kinetics and efficiency in phototrophic green sulfur bacteria [J]. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2018, 1859: 1180-1190. 

[54] QIN X, SUGA M, KUANG T, et al. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex [J]. Science, 2015, 348: 989-995. 

[55] MAZOR Y, BOROVIKOVA A, CASPY I, et al. Structure of the plant photosystem I supercomplex at 2.6 Å resolution [J]. Nature Plants, 2017, 3: 17014. DOI: 10.1038/nplants.2017.14. 

[56] MÜH F, MADJET M E, ADOLPHS J, et al. α-helices direct excitation energy flow in the Fenna-Matthews-Olson protein [J]. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104: 16862-16867.

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