Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I.


Journal

Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677

Informations de publication

Date de publication:
06 2019
Historique:
received: 13 11 2018
accepted: 02 05 2019
entrez: 12 6 2019
pubmed: 12 6 2019
medline: 28 8 2019
Statut: ppublish

Résumé

In plants and green algae, the core of photosystem I (PSI) is surrounded by a peripheral antenna system consisting of light-harvesting complex I (LHCI). Here we report the cryo-electron microscopic structure of the PSI-LHCI supercomplex from the green alga Chlamydomonas reinhardtii. The structure reveals that eight Lhca proteins form two tetrameric LHCI belts attached to the PsaF side while the other two Lhca proteins form an additional Lhca2/Lhca9 heterodimer attached to the opposite side. The spatial arrangement of light-harvesting pigments reveals that Chlorophylls b are more abundant in the outer LHCI belt than in the inner LHCI belt and are absent from the core, thereby providing the downhill energy transfer pathways to the PSI core. PSI-LHCI is complexed with a plastocyanin on the patch of lysine residues of PsaF at the luminal side. The assembly provides a structural basis for understanding the mechanism of light-harvesting, excitation energy transfer of the PSI-LHCI supercomplex and electron transfer with plastocyanin.

Identifiants

pubmed: 31182847
doi: 10.1038/s41477-019-0438-4
pii: 10.1038/s41477-019-0438-4
doi:

Substances chimiques

Light-Harvesting Protein Complexes 0
Membrane Proteins 0
Photosystem I Protein Complex 0
Plastocyanin 9014-09-9

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

626-636

Références

Nelson, N. & Junge, W. Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu. Rev. Biochem. 84, 659–683 (2015).
Suga, M., Qin, X., Kuang, T. & Shen, J. R. Structure and energy transfer pathways of the plant photosystem I-LHCI supercomplex. Curr. Opin. Struct. Biol. 39, 46–53 (2016).
doi: 10.1016/j.sbi.2016.04.004
Nelson, N. Plant photosystem I - the most efficient nano-photochemical machine. J. Nanosci. Nanotechnol. 9, 1709–1713 (2009).
doi: 10.1166/jnn.2009.SI01
Hippler, M., Drepper, F., Haehnel, W. & Rochaix, J. D. The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 95, 7339–7344 (1998).
doi: 10.1073/pnas.95.13.7339
Hippler, M., Drepper, F., Rochaix, J. D. & Muhlenhoff, U. Insertion of the N-terminal part of PsaF from Chlamydomonas reinhardtii into photosystem I from Synechococcus elongatus enables efficient binding of algal plastocyanin and cytochrome c6. J. Biol. Chem. 274, 4180–4188 (1999).
doi: 10.1074/jbc.274.7.4180
Kubota-Kawai, H. et al. X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex. Nat. Plants 4, 218–224 (2018).
doi: 10.1038/s41477-018-0130-0
Blankenship, R. E. Origin and early evolution of photosynthesis. Photosynth. Res. 33, 91–111 (1992).
doi: 10.1007/BF00039173
Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411, 909–917 (2001).
doi: 10.1038/35082000
Mazor, Y., Borovikova, A., Caspy, I. & Nelson, N. Structure of the plant photosystem I supercomplex at 2.6 A resolution. Nat. Plants 3, 17014 (2017).
doi: 10.1038/nplants.2017.14
Qin, X., Suga, M., Kuang, T. & Shen, J. R. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348, 989–995 (2015).
doi: 10.1126/science.aab0214
Mazor, Y., Borovikova, A. & Nelson, N. The structure of plant photosystem I super-complex at 2.8 A resolution. eLife 4, e07433 (2015).
doi: 10.7554/eLife.07433
Pan, X. W., Liu, Z. F., Li, M. & Chang, W. R. Architecture and function of plant light-harvesting complexes II. Curr. Opin. Struct. Biol. 23, 515–525 (2013).
doi: 10.1016/j.sbi.2013.04.004
Drop, B. et al. Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J. Biol. Chem. 286, 44878–44887 (2011).
doi: 10.1074/jbc.M111.301101
Ozawa, S. et al. Configuration of ten light-harvesting chlorophyll a/b complex I subunits in Chlamydomonas reinhardtii photosystem I. Plant Physiol. 178, 583–595 (2018).
Kubota-Kawai, H. et al. Ten antenna proteins are associated with the core in the supramolecular organization of the photosystem I supercomplex in Chlamydomonas reinhardtii. J. Biol. Chem. 294, 4304–4314 (2019).
doi: 10.1074/jbc.RA118.006536
Su, X. et al. Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex. Nat. Plants 5, 273–281 (2019).
doi: 10.1038/s41477-019-0380-5
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
doi: 10.1107/S0907444909042073
Watanabe, A., Kim, E., Burton-Smith, R. N., Tokutsu, R. & Minagawa, J. Amphipol-assisted purification method for the highly active and stable photosystem II supercomplex of Chlamydomonas reinhardtii. FEBS Lett. 593, 1072–1079 (2019).
doi: 10.1002/1873-3468.13394
Ozawa, S., Kosugi, M., Kashino, Y., Sugimura, T. & Takahashi, Y. 5′-Monohydroxyphylloquinone is the dominant naphthoquinone of PSI in the green alga Chlamydomonas reinhardtii . Plant Cell Physiol. 53, 237–243 (2012).
doi: 10.1093/pcp/pcr168
Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428, 287–292 (2004).
doi: 10.1038/nature02373
Pan, X. et al. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat. Struct. Mol. Biol. 18, 309–315 (2011).
doi: 10.1038/nsmb.2008
Wei, X. et al. Structure of spinach photosystem II-LHCII supercomplex at 3.2 A resolution. Nature 534, 69–74 (2016).
doi: 10.1038/nature18020
Bujaldon, S. et al. Functional accumulation of antenna proteins in chlorophyll b-less mutants of Chlamydomonas reinhardtii. Mol. Plant 10, 115–130 (2017).
doi: 10.1016/j.molp.2016.10.001
Qin, X. et al. Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat. Plants 5, 263–272 (2019).
doi: 10.1038/s41477-019-0379-y
Fan, M. et al. Crystal structures of the PsbS protein essential for photoprotection in plants. Nat. Struct. Mol. Biol. 22, 729–735 (2015).
doi: 10.1038/nsmb.3068
Steinbeck, J. et al. Structure of a PSI-LHCI-cyt b6f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions. Proc. Natl Acad. Sci. USA 115, 10517–10522 (2018).
doi: 10.1073/pnas.1809973115
Pi, X. et al. Unique organization of photosystem I-light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc. Natl Acad. Sci. USA 115, 4423–4428 (2018).
doi: 10.1073/pnas.1722482115
Pan, X. et al. Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II. Science 360, 1109–1113 (2018).
doi: 10.1126/science.aat1156
Shimada, S. et al. Complex structure of cytochrome c-cytochrome c oxidase reveals a novel protein-protein interaction mode. EMBO J. 36, 291–300 (2016).
doi: 10.15252/embj.201695021
Fischer, N., Stampacchia, O., Redding, K. & Rochaix, J. D. Selectable marker recycling in the chloroplast. Mol. Gen. Genet. 251, 373–380 (1996).
doi: 10.1007/BF02172529
Kuroda, H., Kodama, N., Sun, X. Y., Ozawa, S. & Takahashi, Y. Requirement for Asn298 on D1 protein for oxygen evolution: analyses by exhaustive amino acid substitution in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol. 55, 1266–1275 (2014).
doi: 10.1093/pcp/pcu073
Ozawa, S. et al. Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21, 2424–2442 (2009).
doi: 10.1105/tpc.108.063313
Chua, N. H. & Bennoun, P. Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl Acad. Sci. USA 72, 2175–2179 (1975).
doi: 10.1073/pnas.72.6.2175
Fling, S. P. & Gregerson, D. S. Peptide and protein molecular weight determination by electrophoresis using a high-molarity Tris buffer system without urea. Anal. Biochem. 155, 83–88 (1986).
doi: 10.1016/0003-2697(86)90228-9
Ozawa, S., Onishi, T. & Takahashi, Y. Identification and characterization of an assembly intermediate subcomplex of photosystem I in the green alga Chlamydomonas reinhardtii. J. Biol. Chem. 285, 20072–20079 (2010).
doi: 10.1074/jbc.M109.098954
Yamano, T. et al. Light and low-CO
doi: 10.1093/pcp/pcq105
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
doi: 10.1038/nmeth.4193
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
doi: 10.1016/j.jsb.2015.11.003
Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
doi: 10.1016/j.jsb.2012.09.006
Pettersen, E. F. et al. UCSF chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
doi: 10.1002/jcc.20084
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
doi: 10.1107/S0907444904019158
Adams, P. D. et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
doi: 10.1107/S0907444909052925

Auteurs

Michihiro Suga (M)

Research Institute for Interdisciplinary Science, Okayama University, Okayama, Japan.
JST, PRESTO, Kawaguchi, Japan.

Shin-Ichiro Ozawa (SI)

Research Institute for Interdisciplinary Science, Okayama University, Okayama, Japan.

Kaori Yoshida-Motomura (K)

Research Institute for Interdisciplinary Science, Okayama University, Okayama, Japan.

Fusamichi Akita (F)

Research Institute for Interdisciplinary Science, Okayama University, Okayama, Japan.
JST, PRESTO, Kawaguchi, Japan.

Naoyuki Miyazaki (N)

Institute for Protein Research, Osaka University, Osaka, Japan. naomiyazaki@protein.osaka-u.ac.jp.
Life Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance, University of Tsukuba, Tsukuba, Japan. naomiyazaki@protein.osaka-u.ac.jp.

Yuichiro Takahashi (Y)

Research Institute for Interdisciplinary Science, Okayama University, Okayama, Japan. taka@cc.okayama-u.ac.jp.

Articles similaires

alpha-Synuclein Humans Animals Mice Lewy Body Disease
Humans Stomach Neoplasms Macrophages Tumor Microenvironment Disease Progression
Animals Humans TOR Serine-Threonine Kinases Lupus Erythematosus, Systemic Arthritis, Rheumatoid

Mutational analysis of Phanerochaete chrysosporium´s purine transporter.

Mariana Barraco-Vega, Manuel Sanguinetti, Gabriela da Rosa et al.
1.00
Phanerochaete Fungal Proteins Purines Aspergillus nidulans DNA Mutational Analysis

Classifications MeSH