Core and rod structures of a thermophilic cyanobacterial light-harvesting phycobilisome.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
17 06 2022
17 06 2022
Historique:
received:
28
10
2021
accepted:
24
05
2022
entrez:
17
6
2022
pubmed:
18
6
2022
medline:
22
6
2022
Statut:
epublish
Résumé
Cyanobacteria, glaucophytes, and rhodophytes utilize giant, light-harvesting phycobilisomes (PBSs) for capturing solar energy and conveying it to photosynthetic reaction centers. PBSs are compositionally and structurally diverse, and exceedingly complex, all of which pose a challenge for a comprehensive understanding of their function. To date, three detailed architectures of PBSs by cryo-electron microscopy (cryo-EM) have been described: a hemiellipsoidal type, a block-type from rhodophytes, and a cyanobacterial hemidiscoidal-type. Here, we report cryo-EM structures of a pentacylindrical allophycocyanin core and phycocyanin-containing rod of a thermophilic cyanobacterial hemidiscoidal PBS. The structures define the spatial arrangement of protein subunits and chromophores, crucial for deciphering the energy transfer mechanism. They reveal how the pentacylindrical core is formed, identify key interactions between linker proteins and the bilin chromophores, and indicate pathways for unidirectional energy transfer.
Identifiants
pubmed: 35715389
doi: 10.1038/s41467-022-30962-9
pii: 10.1038/s41467-022-30962-9
pmc: PMC9205905
doi:
Substances chimiques
Light-Harvesting Protein Complexes
0
Phycobilisomes
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3389Informations de copyright
© 2022. The Author(s).
Références
Sidler, W. A. Phycobilisome and Phycobiliprotein Structures (Advanced Photosynthesis and Respiration, Volume 1, Springer, Dordrecht, 1994), pp. 139–216.
Gan, F. et al. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345, 1312–1317 (2014).
pubmed: 25214622
doi: 10.1126/science.1256963
Li, Y. et al. Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim. Biophys. Acta Bioenerg. 1857, 107–114 (2016).
doi: 10.1016/j.bbabio.2015.10.009
Scheer, H. & Zhao, K. H. Biliprotein maturation: the chromophore attachment. Mol. Microbiol. 68, 263–276 (2008).
pubmed: 18284595
pmcid: 2327270
doi: 10.1111/j.1365-2958.2008.06160.x
Bryant, D. A., Guglielmi, G., de Marsac, N. T., Castets, A. M. & Cohen-Bazire, G. The structure of cyanobacterial phycobilisomes: a model. Arch. Microbiol. 123, 113–127 (1979).
doi: 10.1007/BF00446810
Arteni, A. A., Ajlani, G. & Boekema, E. J. Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane. Biochim. Biophys. Acta Bioenerg. 1787, 272–279 (2009).
doi: 10.1016/j.bbabio.2009.01.009
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
Arteni, A. A. et al. Structure and organization of phycobilisomes on membranes of the red alga Porphyridium cruentum. Photosynth. Res. 95, 169–174 (2008).
pubmed: 17922299
doi: 10.1007/s11120-007-9264-z
Gantt, E. & Lipschultz, C. A. Structure and phycobiliprotein composition of phycobilisomes from Griffithsia pacifica (Rhodophyceae). J. Phycol. 16, 394–398 (1980).
doi: 10.1111/j.1529-8817.1980.tb03051.x
Watanabe, M. et al. Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc. Natl Acad. Sci. USA 111, 2512–2517 (2014).
pubmed: 24550276
pmcid: 3932850
doi: 10.1073/pnas.1320599111
Hirose, Y. et al. Diverse chromatic acclimation processes regulating phycoerythrocyanin and rod-shaped phycobilisome in cyanobacteria. Mol. Plant. 12, 715–725 (2019).
pubmed: 30818037
doi: 10.1016/j.molp.2019.02.010
Marquardt, J., Senger, H., Miyashita, H., Miyachi, S. & Mörschel, E. Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett. 410, 428–432 (1997).
pubmed: 9237676
doi: 10.1016/S0014-5793(97)00631-5
Chen, M., Floetenmeyer, M. & Bibby, T. S. Supramolecular organization of phycobiliproteins in the chlorophyll d-containing cyanobacterium Acaryochloris marina. FEBS Lett. 583, 2535–2539 (2009).
pubmed: 19596002
doi: 10.1016/j.febslet.2009.07.012
Guglielmi, G., Cohen-Bazire, G. & Bryant, D. The structure of Gloeobacter violaceus and its phycobiliosomes. Arch. Microbiol. 129, 181–189 (1981).
doi: 10.1007/BF00425248
Glazer, A. N., Williams, R. C., Yamanaka, G. & Schachman, H. K. Characterization of cyanobacterial phycobilisomes in zwitterionic detergents. Proc. Natl Acad. Sci. USA 76, 6162–6166 (1979).
pubmed: 16592734
pmcid: 411823
doi: 10.1073/pnas.76.12.6162
Cohen-Bazire, G. & Bryant, D. A. Phycobilisomes: composition and structure. In: Carr N. G., Whitton B. A. (eds) The Biology of Cyanobacteria. pp.143–190 (Blackwell, Oxford London,1982).
Glauser, M. et al. Phycobilisome structure in the cyanobacteria Mastigocladus laminosus and Anabaena sp. PCC 7120. Eur. J. Biochem. 205, 907–915 (1992).
pubmed: 1577008
doi: 10.1111/j.1432-1033.1992.tb16857.x
Collier, J. L. & Grossman, A. R. A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J. 13, 1039–1047 (1994).
pubmed: 8131738
pmcid: 394911
doi: 10.1002/j.1460-2075.1994.tb06352.x
Zhang, J. et al. Structure of phycobilisome from the red alga Griffithsia pacifica. Nature 551, 57–63 (2017).
pubmed: 29045394
doi: 10.1038/nature24278
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
Adir, N., Bar-Zvi, S. & Harris, D. The amazing phycobilisome. Biochim. Biophys. Acta Bioenerg. 1861, 148047 (2020).
pubmed: 31306623
doi: 10.1016/j.bbabio.2019.07.002
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
Kosourov, S., Murukesan, G., Seibert, M. & Allahverdiyeva, Y. Evaluation of light energy to H2 energy conversion efficiency in thin films of cyanobacteria and green alga under photoautotrophic conditions. Algal Res. 28, 253–263 (2017).
doi: 10.1016/j.algal.2017.09.027
Santos-Merino, M., Singh, A. K. & Ducat, D. C. New applications of synthetic biology tools for cyanobacterial metabolic engineering. Front. Bioeng. Biotechnol. 7, 1–24 (2019).
doi: 10.3389/fbioe.2019.00033
Kim, M. J. et al. A Broadband multiplex living solar cell. Nano Lett. 20, 4286–4291 (2020).
pubmed: 32365296
doi: 10.1021/acs.nanolett.0c00894
Kawakami, K. et al. Structural implications for a phycobilisome complex from the thermophilic cyanobacterium Thermosynechococcus vulcanus. Biochim. Biophys. Acta Bioenerg. 1862, 148458 (2021).
pubmed: 34062150
doi: 10.1016/j.bbabio.2021.148458
Liu, H. et al. Structure of cyanobacterial phycobilisome core revealed by structural modeling and chemical cross-linking. Sci. Adv. 7, 1–11 (2021).
Zhao, K. H. et al. Phycobilin:cystein-84 biliprotein lyase, a near-universal lyase for cysteine-84-binding sites in cyanobacterial phycobiliproteins. Proc. Natl Acad. Sci. USA 104, 14300–14305 (2007).
pubmed: 17726096
pmcid: 1955460
doi: 10.1073/pnas.0706209104
Nganou, C., David, L., Adir, N. & Mkandawire, M. Linker proteins enable ultrafast excitation energy transfer in the phycobilisome antenna system of Thermosynechococcus vulcanus. Photochem. Photobiol. Sci. 15, 31 (2015).
pubmed: 26537632
doi: 10.1039/c5pp00285k
Hirota, Y. et al. Ultrafast energy transfer dynamics of phycobilisome from Thermosynechococcus vulcanus, as revealed by ps fluorescence and fs pump-probe spectroscopies. Photosynth. Res. https://doi.org/10.1007/s11120-021-00844-0 . (2021).
McGregor, A., Klartag, M., David, L. & Adir, N. Allophycocyanin trimer stability and functionality are primarily due to polar enhanced hydrophobicity of the phycocyanobilin binding pocket. J. Mol. Biol. 384, 406–421 (2008).
pubmed: 18823993
doi: 10.1016/j.jmb.2008.09.018
David, L., Marx, A. & Adir, N. High-resolution crystal structures of trimeric and rod phycocyanin. J. Mol. Biol. 405, 201–213 (2011).
pubmed: 21035460
doi: 10.1016/j.jmb.2010.10.036
Adir, N., Dobrovetsky, Y. & Lerner, N. Structure of c-phycocyanin from the thermophilic cyanobacterium Synechococcus vulcanus at 2.5 Å: structural implications for thermal stability in phycobiliosme assembly. J. Mol. Biol. 313, 71–81 (2001).
Adir, N. & Lerner, N. The crystal structure of a novel unmethylated form of c-phycocyanin, a possible connector between cores and rods in phycobilisomes. J. Biol. Chem. 278, 25926–25932 (2003).
pubmed: 12709431
doi: 10.1074/jbc.M302838200
Murray, J. W., Maghlaoui, K. & Barber, J. The structure of allophycocyanin from Thermosynechococcus elongatus at 3.5 Å resolution. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 63, 998–1002 (2007).
pubmed: 18084078
pmcid: 2344114
doi: 10.1107/S1744309107050920
Marx, A. & Adir, N. Allophycocyanin and phycocyanin crystal structures reveal facets of phycobilisome assembly. Biochim. Biophys. Acta Bioenerg. 1827, 311–318 (2013).
doi: 10.1016/j.bbabio.2012.11.006
David, L. et al. Structural studies show energy transfer within stabilized phycobilisomes independent of the mode of rod-core assembly. Biochim. Biophys. Acta Bioenerg. 1837, 385–395 (2014).
doi: 10.1016/j.bbabio.2013.12.014
Kastner, B. et al. GraFix: sample preparation for single-particle electron cryomicroscopy. Nat. Methods 5, 53–55 (2008).
pubmed: 18157137
doi: 10.1038/nmeth1139
Pintilie, G. et al. Measurement of atom resolvability in cryo-EM maps with Q-scores. Nat. Methods 17, 328–334 (2020).
pubmed: 32042190
pmcid: 7446556
doi: 10.1038/s41592-020-0731-1
Saito, K., Mitsuhashi, K. & Ishikita, H. Dependence of the chlorophyll wavelength on the orientation of a charged group: why does the accessory chlorophyll have a low site energy in photosystem II? J. Photochem. Photobiol. A Chem. 402, 112799 (2020).
doi: 10.1016/j.jphotochem.2020.112799
Förster, T. Zwischenmolecculare Energiewanderung und Fluoreszen, pp. 55–75 (1948).
Stryer, L. & Haugland, R. P. Energy transfer: a spectroscopic ruler. Proc. Natl Acad. Sci. USA 58, 719–726 (1967).
pubmed: 5233469
pmcid: 335693
doi: 10.1073/pnas.58.2.719
Womick, J. M. & Moran, A. M. Exciton coherence and energy transport in the light-harvesting dimers of allophycocyanin. J. Phys. Chem. B. 113, 15747–15759 (2009).
pubmed: 19894754
doi: 10.1021/jp907644h
Womick, J. M. & Moran, A. M. Nature of excited states and relaxation mechanisms in C-Phycocyanin. J. Phys. Chem. B. 113, 15771–15782 (2009).
pubmed: 19902910
doi: 10.1021/jp908093x
Wong, C. Y. et al. Electronic coherence lineshapes reveal hidden excitonic correlations in photosynthetic light harvesting. Nat. Chem. 4, 396–404 (2012).
pubmed: 22522260
doi: 10.1038/nchem.1302
MacColl, R. Allophycocyanin and energy transfer. Biochim. Biophys. Acta Bioenerg. 1657, 73–81 (2004).
doi: 10.1016/j.bbabio.2004.04.005
Soulier, N. & Bryant, D. A. The structural basis of far-red light absorbance by allophycocyanins Photosynth. Res. 147, 11–26 (2021). https://doi.org/10.1007/s11120-020-00787-y .
Zhao, J. Zhou, J. & Bryant, D. A. Energy transfer processes in phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC 7002. N. Murata (Ed.), Research in Photosynthesis, Vol. 1, 25–32 (Kluwer, Dordrecht, 1992).
Dong, C. et al. ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002. Biochim. Biophys. Acta Bioenerg. 1787, 1122–1128 (2009).
doi: 10.1016/j.bbabio.2009.04.007
Ashby, M. K. & Mullineaux, C. W. The role of ApcD and ApcF in energy transfer from phycobilisomes to PS I and PS II in a cyanobacterium. Photosynth. Res. 61, 169–179 (1999).
doi: 10.1023/A:1006217201666
Tang, K. et al. The terminal phycobilisome emitter, LCM: a light-harvesting pigment with a phytochrome chromophore. Proc. Natl Acad. Sci. USA 112, 15880–15885 (2015).
pubmed: 26669441
pmcid: 4702970
doi: 10.1073/pnas.1519177113
Mimuro, M. Studies on excitation energy flow in the photosynthetic pigment system; structure and energy transfer mechanism. Bot. Mag. 103, 233–253 (1990).
doi: 10.1007/BF02489628
Zhang, J., Zhao, F., Zheng, X. & Wang, H. Direct measurement of excitation transfer dynamics between two trimers in C-phycocyanin hexamer from cyanobacterium Anabaena variabilis. Chem. Phys. Lett. 304, 357–364 (1999).
doi: 10.1016/S0009-2614(99)00352-8
Niedzwiedzki, D. M., Bar-Zvi, S., Blankenship, R. E. & Adir, N. Mapping the excitation energy migration pathways in phycobilisomes from the cyanobacterium Acaryochloris marina. Biochim. Biophys. Acta Bioenerg. 1860, 286–296 (2019).
pubmed: 30703363
doi: 10.1016/j.bbabio.2019.01.002
Shen, J.-R., Kawakami, K. & Koike, H. Purification and crystallization of oxygen-evolving photosystem II core complex from thermophilic cyanobacteria. Photosynth. Res. Protoc. 684, 41–51 (2011).
doi: 10.1007/978-1-60761-925-3_5
Kawakami, K. & Shen, J. R. Purification of fully active and crystallizable photosystem II from thermophilic cyanobacteria. Methods Enzymol. 613, 1–16 (2018).
pubmed: 30509462
doi: 10.1016/bs.mie.2018.10.002
Zivanov, J., Nakane, T. & Scheres, S. H. W. Estimation of high-order aberrations and anisotropic magnification from cryo-EM data sets in RELION-3.1. IUCrJ 7, 253–267 (2020).
pubmed: 32148853
pmcid: 7055373
doi: 10.1107/S2052252520000081
Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
pubmed: 26278980
pmcid: 6760662
doi: 10.1016/j.jsb.2015.08.008
de la Rosa-Trevín, J. M. et al. Xmipp 3.0: an improved software suite for image processing in electron microscopy. J. Struct. Biol. 184, 321–328 (2013).
pubmed: 24075951
doi: 10.1016/j.jsb.2013.09.015
Zhang, J. et al. JADAS: a customizable automated data acquisition system and its application to ice-embedded single particles. J. Struct. Biol. 165, 1–9 (2009).
pubmed: 18926912
doi: 10.1016/j.jsb.2008.09.006
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 5494038
doi: 10.1038/nmeth.4193
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473
doi: 10.1038/nmeth.4169
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
pubmed: 26592709
pmcid: 4711343
doi: 10.1016/j.jsb.2015.11.003
Bell, J. M., Chen, M., Durmaz, T., Fluty, A. C. & Ludtke, S. J. New software tools in EMAN2 inspired by EMDatabank map challenge. J. Struct. Biol. 204, 283–290 (2018).
pubmed: 30189321
pmcid: 6163079
doi: 10.1016/j.jsb.2018.09.002
Rohou, A., Grant, T. & Grigorieff, N. cis TEM, user-friendly software for single-particle image processing. Elife 7, e35383 (2018).
pubmed: 29513216
pmcid: 5854467
doi: 10.7554/eLife.35383
Moriarty, N. W., Grosse-Kunstleve, R. W. & Adams, P. D. Electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation. Acta Crystallogr. Sect. D. Biol. Crystallogr. 65, 1074–1080 (2009).
doi: 10.1107/S0907444909029436
Ramírez-Aportela, E. et al. FSC-Q: a CryoEM map-to-atomic model quality validation based on the local Fourier shell correlation. Nat. Commun. 12, 1–7 (2021).
doi: 10.1038/s41467-020-20295-w
Yang, Y. et al. Active and silent chromophore isoforms for phytochrome Pr photoisomerization: an alternative evolutionary strategy to optimize photoreaction quantum yields. Struct. Dyn. 1, 014701 (2014).
pubmed: 26798771
pmcid: 4711594
doi: 10.1063/1.4865233
Hellman, U., Wernstedt, C., Góñez, J. & Heldin, C. H. Improvement of an “in-gel” digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224, 451–455 (1995).
pubmed: 7710111
doi: 10.1006/abio.1995.1070
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).
pubmed: 29077904
doi: 10.1093/molbev/msx281