Structure and distinct supramolecular organization of a PSII-ACPII dimer from a cryptophyte alga Chroomonas placoidea.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
28 May 2024
28 May 2024
Historique:
received:
29
11
2023
accepted:
15
05
2024
medline:
29
5
2024
pubmed:
29
5
2024
entrez:
28
5
2024
Statut:
epublish
Résumé
Cryptophyte algae are an evolutionarily distinct and ecologically important group of photosynthetic unicellular eukaryotes. Photosystem II (PSII) of cryptophyte algae associates with alloxanthin chlorophyll a/c-binding proteins (ACPs) to act as the peripheral light-harvesting system, whose supramolecular organization is unknown. Here, we purify the PSII-ACPII supercomplex from a cryptophyte alga Chroomonas placoidea (C. placoidea), and analyze its structure at a resolution of 2.47 Å using cryo-electron microscopy. This structure reveals a dimeric organization of PSII-ACPII containing two PSII core monomers flanked by six symmetrically arranged ACPII subunits. The PSII core is conserved whereas the organization of ACPII subunits exhibits a distinct pattern, different from those observed so far in PSII of other algae and higher plants. Furthermore, we find a Chl a-binding antenna subunit, CCPII-S, which mediates interaction of ACPII with the PSII core. These results provide a structural basis for the assembly of antennas within the supercomplex and possible excitation energy transfer pathways in cryptophyte algal PSII, shedding light on the diversity of supramolecular organization of photosynthetic machinery.
Identifiants
pubmed: 38806516
doi: 10.1038/s41467-024-48878-x
pii: 10.1038/s41467-024-48878-x
doi:
Substances chimiques
Photosystem II Protein Complex
0
Chlorophyll
1406-65-1
Chlorophyll Binding Proteins
0
Chlorophyll A
YF5Q9EJC8Y
Light-Harvesting Protein Complexes
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4535Informations de copyright
© 2024. The Author(s).
Références
Nelson, N. & Junge, W. Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu. Rev. Biochem. 84, 659–683 (2015).
pubmed: 25747397
doi: 10.1146/annurev-biochem-092914-041942
Barber, J. Photosystem II: the engine of life. Q. Rev. Biophys. 36, 71–89 (2003).
pubmed: 12643043
doi: 10.1017/S0033583502003839
Shen, J.-R. The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu. Rev. Plant Biol. 66, 23–48 (2015).
pubmed: 25746448
doi: 10.1146/annurev-arplant-050312-120129
Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Crystal structure of oxygen evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–60 (2011).
pubmed: 21499260
doi: 10.1038/nature09913
Cao, P., Pan, X., Su, X., Liu, Z. & Li, M. Assembly of eukaryotic photosystem II with diverse light-harvesting antennas. Curr. Opin. Struct. Biol. 63, 49–57 (2020).
pubmed: 32389895
doi: 10.1016/j.sbi.2020.03.007
Croce, R. & van Amerongen, H. Natural strategies for photosynthetic light harvesting. Nat. Chem. Biol. 10, 492–501 (2014).
pubmed: 24937067
doi: 10.1038/nchembio.1555
Croce, R. & van Amerongen, H. Light harvesting in oxygenic photosynthesis: structural biology meets spectroscopy. Science 369, eaay2058 (2020).
pubmed: 32820091
doi: 10.1126/science.aay2058
Chang, L. et al. Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res 25, 726–737 (2015).
pubmed: 25998682
pmcid: 4456626
doi: 10.1038/cr.2015.59
Zheng, L. et al. Structural insight into the mechanism of energy transfer in cyanobacterial phycobilisomes. Nat. Commun. 12, 5497 (2021).
pubmed: 34535665
pmcid: 8448738
doi: 10.1038/s41467-021-25813-y
Ma, J. et al. Structural basis of energy transfer in Porphyridium purpureum phycobilisome. Nature 579, 146–151 (2020).
pubmed: 32076272
doi: 10.1038/s41586-020-2020-7
Zhang, J. et al. Structure of phycobilisome from the red alga Griffithsia pacifica. Nature 551, 57–63 (2017).
pubmed: 29045394
doi: 10.1038/nature24278
You, X. et al. In situ structure of the red algal phycobilisome-PSII-PSI-LHC megacomplex. Nature 616, 199–206 (2023).
pubmed: 36922595
doi: 10.1038/s41586-023-05831-0
Shen, L. et al. Structure of a C
pubmed: 31570614
pmcid: 6800332
doi: 10.1073/pnas.1912462116
Sheng, X. et al. Structural insight into light harvesting for photosystem II in green algae. Nat. Plants 5, 1320–1330 (2019).
pubmed: 31768031
doi: 10.1038/s41477-019-0543-4
Pi, X. et al. The pigment-protein network of a diatom photosystem II-light-harvesting antenna supercomplex. Science 365, eaax4406 (2019).
pubmed: 31371578
doi: 10.1126/science.aax4406
Nagao, R. et al. Structural basis for different types of hetero-tetrameric light-harvesting complexes in a diatom PSII-FCPII supercomplex. Nat. Commun. 13, 1764 (2022).
pubmed: 35365610
pmcid: 8976053
doi: 10.1038/s41467-022-29294-5
Wei, X. et al. Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution. Nature 534, 69–74 (2016).
pubmed: 27251276
doi: 10.1038/nature18020
Su, X. et al. Structure and assembly mechanism of plant C
pubmed: 28839073
doi: 10.1126/science.aan0327
Mendes, C. R. B. et al. Cryptophytes: an emerging algal group in the rapidly changing Antarctic Peninsula marine environments. Glob. Chang. Biol. 29, 1791–1808 (2023).
pubmed: 36656050
doi: 10.1111/gcb.16602
Kim, J. I. et al. Evolutionary dynamics of cryptophyte plastid genomes. Genome Biol. Evol. 9, 1859–1872 (2017).
pubmed: 28854597
pmcid: 5534331
doi: 10.1093/gbe/evx123
Falkowski, P. G. et al. The evolution of modern eukaryotic phytoplankton. Science 305, 354–360 (2004).
pubmed: 15256663
doi: 10.1126/science.1095964
Burki, F., Okamoto, N., Pombert, J. F. & Keeling, P. J. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc. Biol. Sci. 279, 2246–2254 (2012).
pubmed: 22298847
pmcid: 3321700
Zimorski, V., Ku, C., Martin, W. F. & Gould, S. B. Endosymbiotic theory for organelle origins. Curr. Opin. Microbiol. 22, 38–48 (2014).
pubmed: 25306530
doi: 10.1016/j.mib.2014.09.008
Stiller, J. W. et al. The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat. Commun. 5, 5764 (2014).
pubmed: 25493338
doi: 10.1038/ncomms6764
Greenwold, M. J. et al. Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae. Proc. Biol. Sci. 286, 20190655 (2019).
pubmed: 31088271
pmcid: 6532512
Overkamp, K. E. et al. Insights into the biosynthesis and assembly of cryptophycean phycobiliproteins. J. Biol. Chem. 289, 26691–26707 (2014).
pubmed: 25096577
pmcid: 4175312
doi: 10.1074/jbc.M114.591131
Spear-Bernstein, L. & Miller, K. R. Unique location of the phycobiliprotein light-harvesting pigment in the Cryptophyceae. J. Phycol. 25, 412–419 (1989).
doi: 10.1111/j.1529-8817.1989.tb00245.x
Neilson, J. A. & Durnford, D. G. Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth. Res. 106, 57–71 (2010).
pubmed: 20596891
doi: 10.1007/s11120-010-9576-2
Büchel, C. Light harvesting complexes in chlorophyll c-containing algae. Biochim. Biophys. Acta Bioenerg. 1861, 148027 (2020).
pubmed: 31153887
doi: 10.1016/j.bbabio.2019.05.003
Kereiche, S. et al. Association of chlorophyll a/c(2) complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24. Biochim. Biophys. Acta 1777, 1122–1128 (2008).
pubmed: 18513489
doi: 10.1016/j.bbabio.2008.04.045
Kuthanová Trsková, E. et al. Isolation and characterization of CAC antenna proteins and photosystem I supercomplex from the cryptophytic alga Rhodomonas salina. Physiol. Plant. 166, 309–319 (2019).
pubmed: 30677144
doi: 10.1111/ppl.12928
Zhao, L. S. et al. Structural basis and evolution of the photosystem I-light-harvesting supercomplex of cryptophyte algae. Plant Cell 35, 2449–2463 (2023).
pubmed: 36943796
pmcid: 10291030
doi: 10.1093/plcell/koad087
Suga, M. et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517, 99–103 (2015).
pubmed: 25470056
doi: 10.1038/nature13991
Ago, H. et al. Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J. Biol. Chem. 291, 5676–5687 (2016).
pubmed: 26757821
pmcid: 4786707
doi: 10.1074/jbc.M115.711689
Kaňa, R., Kotabová, E., Sobotka, R. & Prášil, O. Non-photochemical quenching in cryptophyte alga Rhodomonas salina is located in chlorophyll a/c antennae. PLoS One 7, e45645 (2012).
doi: 10.1371/journal.pone.0029700
Funk, C., Alami, M., Tibiletti, T. & Green, B. R. High light stress and the one-helix LHC-like proteins of the cryptophyte Guillardia theta. Biochim. Biophys. Acta Bioenerg. 1807, 841–846 (2011).
doi: 10.1016/j.bbabio.2011.03.011
West, R. et al. Spectroscopic properties of the triple bond carotenoid alloxanthin. Chem. Phys. Lett. 653, 167–172 (2016).
doi: 10.1016/j.cplett.2016.04.085
Šebelík, V. et al. Energy transfer pathways in the CAC light-harvesting complex of Rhodomonas salina. Biochim. Biophys. Acta Bioenerg. 1861, 148280 (2020).
pubmed: 32717221
doi: 10.1016/j.bbabio.2020.148280
Snyder, U. K. & Biggins, J. Excitation-energy redistribution in the cryptomonad alga Cryptomonas ovata. Biochim. Biophys. Acta Bioenerg. 892, 48–55 (1987).
doi: 10.1016/0005-2728(87)90246-5
Cheregi, O. et al. Presence of state transitions in the cryptophyte alga Guillardia theta. J. Exp. Bot. 66, 6461–6470 (2015).
pubmed: 26254328
pmcid: 4588893
doi: 10.1093/jxb/erv362
Jeffrey, S. T. & Humphrey, G. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191–194 (1975).
doi: 10.1016/S0015-3796(17)30778-3
Ikeuchi, M. & Inoue, Y. A new 4.8-kDa polypeptide intrinsic to the PS II reaction center, as revealed by modified SDS-PAGE with improved resolution of low-molecular-weight proteins. Plant Cell Physiol. 29, 1233–1239 (1988).
Punjani, A. et al. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473
doi: 10.1038/nmeth.4169
Wagner, T. et al. SPHIRE-crYOLO is a fast and accurate fully automated particle picker for cryo-EM. Commun. Biol. 2, 218 (2019).
pubmed: 31240256
pmcid: 6584505
doi: 10.1038/s42003-019-0437-z
Bepler, T. et al. Positive-unlabeled convolutional neural networks for particle picking in cryo-electron micrographs. Nat. Methods 16, 1153–1160 (2019).
pubmed: 31591578
pmcid: 6858545
doi: 10.1038/s41592-019-0575-8
Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925
Schrödinger, L. L. C. The PyMOL Molecular Graphics System, Version 2.5.0 (2021).
Mazor, Y., Borovikova, A., Caspy, I. & Nelson, N. Structure of the plant photosystem I supercomplex at 2.6 Å resolution. Nat. Plants 3, 17014 (2017).
pubmed: 28248295
doi: 10.1038/nplants.2017.14
Gradinaru, C. C. et al. The flow of excitation energy in LHCII monomers: implications for the structural model of the major plant antenna. Biophys. J. 75, 3064–3077 (1998).
pubmed: 9826626
pmcid: 1299977
doi: 10.1016/S0006-3495(98)77747-1
Kim, E. Computational analysis of Förster resonance energy transfer in photosynthetic proteins (v1.0.0). Zenodo https://doi.org/10.5281/zenodo.3250649 (2019).