Growth phase-dependent reorganization of cryptophyte photosystem I antennae.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
11 May 2024
11 May 2024
Historique:
received:
22
12
2023
accepted:
30
04
2024
medline:
12
5
2024
pubmed:
12
5
2024
entrez:
11
5
2024
Statut:
epublish
Résumé
Photosynthetic cryptophytes are eukaryotic algae that utilize membrane-embedded chlorophyll a/c binding proteins (CACs) and lumen-localized phycobiliproteins (PBPs) as their light-harvesting antennae. Cryptophytes go through logarithmic and stationary growth phases, and may adjust their light-harvesting capability according to their particular growth state. How cryptophytes change the type/arrangement of the photosynthetic antenna proteins to regulate their light-harvesting remains unknown. Here we solve four structures of cryptophyte photosystem I (PSI) bound with CACs that show the rearrangement of CACs at different growth phases. We identify a cryptophyte-unique protein, PsaQ, which harbors two chlorophyll molecules. PsaQ specifically binds to the lumenal region of PSI during logarithmic growth phase and may assist the association of PBPs with photosystems and energy transfer from PBPs to photosystems.
Identifiants
pubmed: 38734819
doi: 10.1038/s42003-024-06268-5
pii: 10.1038/s42003-024-06268-5
doi:
Substances chimiques
Photosystem I Protein Complex
0
Light-Harvesting Protein Complexes
0
Chlorophyll
1406-65-1
Chlorophyll Binding Proteins
0
Phycobiliproteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
560Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 31930064
Organisme : Chinese Academy of Sciences (CAS)
ID : XDB37020101
Informations de copyright
© 2024. The Author(s).
Références
Stadnichuk, I. N. & Kusnetsov, V. V. Phycobilisomes and phycobiliproteins in the pigment apparatus of oxygenic photosynthetics: from cyanobacteria to tertiary endosymbiosis. Int. J. Mol. Sci. 24, 2290 (2023).
Rakhimberdieva, M. G., Boichenko, V. A., Karapetyan, N. V. & Stadnichuk, I. N. Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium spirulina platensis. Biochemistry 40, 15780–15788 (2001).
doi: 10.1021/bi010009t
pubmed: 11747455
Liu, H. et al. Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342, 1104–1107 (2013).
doi: 10.1126/science.1242321
pubmed: 24288334
pmcid: 3947847
Gantt, E., Grabowski, B. & Cunningham, F. X. Antenna systems of red algae: phycobilisomes with photosystem II and chlorophyll complexes with photosystem. In Light-harvesting antennas in photosynthesis Vol 15, 307–322 (Kluwer Academics, Netherlands, 2003).
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
pubmed: 29632169
pmcid: 5924924
Rochaix, J. D. & Bassi, R. LHC-like proteins involved in stress responses and biogenesis/repair of the photosynthetic apparatus. Biochem. J. 476, 581–593 (2019).
doi: 10.1042/BCJ20180718
pubmed: 30765616
Delwiche, C. F. & Palmer, J. D. The origin of plastids and their spread via secondary symbiosis. In Plant Systematics and Evolution Vol 11, 53–86 (Springer, Vienna, 1997).
Durnford, D. G. et al. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 48, 59–68 (1999).
doi: 10.1007/PL00006445
pubmed: 9873077
Wilk, K. E. et al. Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: crystal structure of a cryptophyte phycoerythrin at 1.63-A resolution. Proc. Natl Acad. Sci. USA 96, 8901–8906 (1999).
doi: 10.1073/pnas.96.16.8901
pubmed: 10430868
pmcid: 17705
Harrop, S. J. et al. Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins. Proc. Natl Acad. Sci. USA 111, E2666–E2675 (2014).
doi: 10.1073/pnas.1402538111
pubmed: 24979784
pmcid: 4084447
Ludwig, M. & Gibbs, S. P. Localization of phycoerythrin at the lumenal surface of the thylakoid membrane in rhodomonas lens. J. Cell Biol. 108, 875–884 (1989).
doi: 10.1083/jcb.108.3.875
pubmed: 2921285
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).
Hoffman, G. E., Sanchez Puerta, M. V. & Delwiche, C. F. Evolution of light-harvesting complex proteins from Chl c-containing algae. BMC Evol. Biol. 11, 101 (2011).
doi: 10.1186/1471-2148-11-101
pubmed: 21496217
pmcid: 3096602
Cheregi, O. et al. Presence of state transitions in the cryptophyte alga Guillardia theta. J. Exp. Bot. 66, 6461–6470 (2015).
doi: 10.1093/jxb/erv362
pubmed: 26254328
pmcid: 4588893
Maltsev, Y., Maltseva, K., Kulikovskiy, M. & Maltseva, S. Influence of light conditions on microalgae growth and content of lipids, carotenoids, and fatty acid composition. Biology (Basel) 10, 1060 (2021).
Kana, R., Kotabova, E., Sobotka, R. & Prasil, O. Non-photochemical quenching in cryptophyte alga Rhodomonas salina is located in chlorophyll a/c antennae. PLoS One 7, e29700 (2012).
doi: 10.1371/journal.pone.0029700
pubmed: 22235327
pmcid: 3250475
Cunningham, B. R. et al. Light capture and pigment diversity in marine and freshwater cryptophytes. J. Phycol. 55, 552–564 (2019).
doi: 10.1111/jpy.12816
pubmed: 30468692
Heidenreich, K. M. & Richardson, T. L. Photopigment, absorption, and growth responses of marine cryptophytes to varying spectral irradiance. J. Phycol. 56, 507–520 (2020).
doi: 10.1111/jpy.12962
pubmed: 31876286
Khrouchtchova, A. et al. A previously found thylakoid membrane protein of 14kDa (TMP14) is a novel subunit of plant photosystem I and is designated PSI-P. FEBS Lett. 579, 4808–4812 (2005).
doi: 10.1016/j.febslet.2005.07.061
pubmed: 16109415
Xu, C. et al. Structural basis for energy transfer in a huge diatom PSI-FCPI supercomplex. Nat. Commun. 11, 5081 (2020).
doi: 10.1038/s41467-020-18867-x
pubmed: 33033236
pmcid: 7545214
Bai, T., Guo, L., Xu, M. & Tian, L. Structural diversity of photosystem I and Its light-harvesting system in eukaryotic algae and plants. Front. Plant Sci. 12, 781035 (2021).
doi: 10.3389/fpls.2021.781035
pubmed: 34917114
pmcid: 8669154
Engelken, J., Brinkmann, H. & Adamska, I. Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol. Biol. 10, 233 (2010).
doi: 10.1186/1471-2148-10-233
pubmed: 20673336
pmcid: 3020630
Ifuku, K. The PsbP and PsbQ family proteins in the photosynthetic machinery of chloroplasts. Plant Physiol. Biochem. 81, 108–114 (2014).
doi: 10.1016/j.plaphy.2014.01.001
pubmed: 24477118
Kana, R., Prasil, O. & Mullineaux, C. W. Immobility of phycobilins in the thylakoid lumen of a cryptophyte suggests that protein diffusion in the lumen is very restricted. FEBS Lett. 583, 670–674 (2009).
doi: 10.1016/j.febslet.2009.01.016
pubmed: 19166839
Douglas, S. E. Eukaryote-eukaryote endosymbioses: insights from studies of a cryptomonad alga. Biosystems 28, 57–68 (1992).
doi: 10.1016/0303-2647(92)90008-M
pubmed: 1292667
You, X. et al. In situ structure of the red algal phycobilisome-PSII-PSI-LHC megacomplex. Nature 616, 199–206 (2023).
doi: 10.1038/s41586-023-05831-0
pubmed: 36922595
Yamamoto, S., Bossier, P. & Yoshimatsu, T. Biochemical characterization of rhodomonas sp. Hf-1 strain (cryptophyte) under nitrogen starvation. Aquaculture 516, 734648 (2020).
van der Weij-De Wit, C. D. et al. How energy funnels from the phycoerythrin antenna complex to photosystem I and photosystem II in cryptophyte rhodomonas CS24 cells. J. Phys. Chem. B 110, 25066–25073 (2006).
doi: 10.1021/jp061546w
pubmed: 17149931
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).
doi: 10.1016/j.bbabio.2008.04.045
pubmed: 18513489
Stadnichuk, I. N. et al. Phycoerythrin association with photosystem II in the cryptophyte alga rhodomonas salina. Biochem. (Mosc.) 85, 679–688 (2020).
doi: 10.1134/S000629792006005X
Sebelik, V., West, R., Trskova, E. K., Kana, R. & Polivka, T. Energy transfer pathways in the CAC light-harvesting complex of rhodomonas salina. Biochim. Biophys. Acta Bioenerg. 1861, 148280 (2020).
doi: 10.1016/j.bbabio.2020.148280
pubmed: 32717221
Guillard, R. R. & Ryther, J. H. Studies of marine planktonic diatoms. I. Cyclotella nana hustedt, and detonula confervacea (cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962).
doi: 10.1139/m62-029
pubmed: 13902807
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
pubmed: 1056023
pmcid: 432719
Wright, S. W. & Jeffrey, S. W. Pigment markers for phytoplankton production. Marine organic matter: biomarkers, isotopes and DNA 2N, 71–104 (2006).
Roy, S., Llewellyn, C. A., Egeland, E. S. & Johnsen, G. Phytoplankton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography 165–236 (Cambridge University Press, 2011).
Chen, Y. et al. SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. GigaScience 7, 1–6 (2018).
doi: 10.1093/gigascience/gix120
pubmed: 29659813
pmcid: 5827348
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
doi: 10.1038/nbt.1883
pubmed: 21572440
pmcid: 3571712
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with bowtie 2. Nat. Methods 9, 357–359 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 3322381
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma. 12, 323 (2011).
doi: 10.1186/1471-2105-12-323
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
pubmed: 28250466
pmcid: 5494038
Zhang, K. Gctf: Real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
doi: 10.1016/j.jsb.2015.11.003
pubmed: 26592709
pmcid: 4711343
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
pubmed: 23000701
pmcid: 3690530
Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63–65 (2014).
doi: 10.1038/nmeth.2727
pubmed: 24213166
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
pubmed: 15264254
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D. Biol. Crystallogr. 66, 213–221 (2010).
doi: 10.1107/S0907444909052925
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. Sect. D. Biol. Crystallogr. 66, 486–501 (2010).
doi: 10.1107/S0907444910007493
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. Sect. D. Biol. Crystallogr. 66, 12–21 (2010).
doi: 10.1107/S0907444909042073