Growth Phase-dependent Reorganization of Cryptophyte Photosystem I Antennae

Overview

Journal Commun Biol

Specialty Biology

Date 2024 May 11

PMID 38734819

Authors

Shumeng Zhang

Long Si

Xiaodong Su

Xuelin Zhao

Xiaomin An

Mei Li

Affiliations

Soon will be listed here.

Abstract

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.

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References

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. 2021; 12:781035. PMC: 8669154. DOI: 10.3389/fpls.2021.781035. View

Ludwig M, Gibbs S . Localization of phycoerythrin at the lumenal surface of the thylakoid membrane in Rhodomonas lens. J Cell Biol. 1989; 108(3):875-84. PMC: 2115399. DOI: 10.1083/jcb.108.3.875. View

Kereiche S, Kouril R, Oostergetel G, Fusetti F, Boekema E, Doust A . Association of chlorophyll a/c(2) complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24. Biochim Biophys Acta. 2008; 1777(9):1122-8. DOI: 10.1016/j.bbabio.2008.04.045. View

Kucukelbir A, Sigworth F, Tagare H . Quantifying the local resolution of cryo-EM density maps. Nat Methods. 2013; 11(1):63-5. PMC: 3903095. DOI: 10.1038/nmeth.2727. View

Hoffman G, Sanchez Puerta M, Delwiche C . Evolution of light-harvesting complex proteins from Chl c-containing algae. BMC Evol Biol. 2011; 11:101. PMC: 3096602. DOI: 10.1186/1471-2148-11-101. View

Khrouchtchova A, Hansson M, Paakkarinen V, Vainonen J, Zhang S, Jensen P . A previously found thylakoid membrane protein of 14kDa (TMP14) is a novel subunit of plant photosystem I and is designated PSI-P. FEBS Lett. 2005; 579(21):4808-12. DOI: 10.1016/j.febslet.2005.07.061. View

Li B, Dewey C . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323. PMC: 3163565. DOI: 10.1186/1471-2105-12-323. View

Chua N, Bennoun P . Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc Natl Acad Sci U S A. 1975; 72(6):2175-9. PMC: 432719. DOI: 10.1073/pnas.72.6.2175. View

Zheng S, Palovcak E, Armache J, Verba K, Cheng Y, Agard D . MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat Methods. 2017; 14(4):331-332. PMC: 5494038. DOI: 10.1038/nmeth.4193. View

10.

Cunningham B, Greenwold M, Lachenmyer E, Heidenreich K, Davis A, Dudycha J . Light capture and pigment diversity in marine and freshwater cryptophytes. J Phycol. 2018; 55(3):552-564. DOI: 10.1111/jpy.12816. View

11.

Ifuku K . The PsbP and PsbQ family proteins in the photosynthetic machinery of chloroplasts. Plant Physiol Biochem. 2014; 81:108-14. DOI: 10.1016/j.plaphy.2014.01.001. View

12.

Scheres S . RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol. 2012; 180(3):519-30. PMC: 3690530. DOI: 10.1016/j.jsb.2012.09.006. View

13.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View

14.

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. 2012; 7(1):e29700. PMC: 3250475. DOI: 10.1371/journal.pone.0029700. View

15.

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

16.

Zhang K . Gctf: Real-time CTF determination and correction. J Struct Biol. 2015; 193(1):1-12. PMC: 4711343. DOI: 10.1016/j.jsb.2015.11.003. View

17.

Guillard R, Ryther J . Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol. 1962; 8:229-39. DOI: 10.1139/m62-029. View

18.

Chen V, Arendall 3rd W, Headd J, Keedy D, Immormino R, Kapral G . MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr. 2010; 66(Pt 1):12-21. PMC: 2803126. DOI: 10.1107/S0907444909042073. View

19.

Sebelik V, West R, Trskova E, Kana R, Polivka T . Energy transfer pathways in the CAC light-harvesting complex of Rhodomonas salina. Biochim Biophys Acta Bioenerg. 2020; 1861(11):148280. DOI: 10.1016/j.bbabio.2020.148280. View

20.

Pi X, Tian L, Dai H, Qin X, Cheng L, Kuang T . Unique organization of photosystem I-light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc Natl Acad Sci U S A. 2018; 115(17):4423-4428. PMC: 5924924. DOI: 10.1073/pnas.1722482115. View