Diatoms are a large group of marine algae that are responsible for about one-quarter of global carbon fixation. Light-harvesting complexes of diatoms are formed by the fucoxanthin chlorophyll a/c proteins and their overall organization around core complexes of photosystems (PSs) I and II is unique in the plant kingdom. Using cryo-electron tomography, we have elucidated the structural organization of PSII and PSI supercomplexes and their spatial segregation in the thylakoid membrane of the model diatom species Thalassiosira pseudonana. 3D sub-volume averaging revealed that the PSII supercomplex of T. pseudonana incorporates a trimeric form of light-harvesting antenna, which differs from the tetrameric antenna observed previously in another diatom, Chaetoceros gracilis. Surprisingly, the organization of the PSI supercomplex is conserved in both diatom species. These results strongly suggest that different diatom classes have various architectures of PSII as an adaptation strategy, whilst a convergent evolution occurred concerning PSI and the overall plastid structure.

Department of Biophysics Faculty of Science Centre of the Region Haná for Biotechnological and Agricultural Research Palacký University Olomouc 78371 Czech Republic

Electron Microscopy Group Groningen Biomolecular Sciences and Biotechnology Institute University of Groningen Groningen 9747AG The Netherlands

Institute for Molecular Biosciences Goethe University of Frankfurt Frankfurt 60438 Germany

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Alegria-Schaffer A, Lodge A, Vattem K (2009) Performing and optimizing western blots with an emphasis on chemiluminescent detection. Methods Enzymol 463: 573–599 PubMed

Andersen B, Scheller HV, Møller BL (1992) The PSI-E subunit of photosystem I binds ferredoxin: NADP+ oxidoreductase. FEBS Lett 311: 169–173 PubMed

Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, et al. (2004) The genome of the diatom Thalassiosira Pseudonana: ecology, evolution, and metabolism. Science 306: 79–86 PubMed

Bedoshvili YD, Popkova TP, Likhoshway YV. (2009) Chloroplast structure of diatoms of different classes. Cell Tissue Biol 3: 297–310

Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426: 630–635 PubMed

van den Berg TE, Arshad R, Nawrocki WJ, Boekema EJ, Kouřil R, Croce R (2020) PSI of the colonial alga Botryococcus braunii has an unusually large antenna size. Plant Physiol 184: 2040–2051 PubMed PMC

Van Bezouwen LS, Caffarri S, Kale R, Kouřil R, Thunnissen AMWH, Oostergetel GT, Boekema EJ (2017) Subunit and chlorophyll organization of the plant photosystem II supercomplex. Nat Plants 3: 17080. PubMed

Bhattacharya D, Archibald JM, Weber APM, Reyes-Prieto A (2007) How do endosymbionts become organelles? Understanding early events in plastid evolution. BioEssays 29: 1239–1246 PubMed

Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93–99

Bozarth A, Maier UG, Zauner S (2009) Diatoms in biotechnology: modern tools and applications. Appl Microbiol Biotechnol 82: 195–201 PubMed

Büchel C (2020) Light harvesting complexes in chlorophyll c-containing algae. Biochim Biophys Acta Bioenerg 1861: 148027. PubMed

Calvaruso C, Rokka A, Aro EM, Büchela C (2020) Specific Lhc proteins are bound to PSI or PSII supercomplexes in the diatom Thalassiosira pseudonana. Plant Physiol 183: 67–79 PubMed PMC

Cao P, Pan X, Su X, Liu Z, Li M (2020) Assembly of eukaryotic photosystem II with diverse light-harvesting antennas. Curr Opin Struct Biol 63: 49–57 PubMed

Caspy I, Borovikova-Sheinker A, Klaiman D, Shkolnisky Y, Nelson N (2020) The structure of a triple complex of plant photosystem I with ferredoxin and plastocyanin. Nat Plants 6: 1300–1305 PubMed

Crowther RA, Derosier DJ, Klug A (1970) The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. Proc Roy Soc Loud A Royal Soc Lond 317: 319–340

Daum B, Nicastro D, Austin J, Richard McIntosh J, Kühlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22: 1299–1312 PubMed PMC

Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta Bioenerg 1706: 12–39 PubMed

Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281: 200–206 PubMed

Flori S, Jouneau PH, Bailleul B, Gallet B, Estrozi LF, Moriscot C, Bastien O, Eicke S, Schober A, Bártulos CR, et al. (2017) Plastid thylakoid architecture optimizes photosynthesis in diatoms. Nat Commun 8: 15885. PubMed PMC

Gantt E, Grabowski B, Cunningham FX (2003) Antenna systems of red algae: phycobilisomes with photosystem ll and chlorophyll complexes with photosystem I. Light-Harvesting Antennas in Photosynthesis. Springer, Dordrecht, pp 307–322

Grouneva I, Rokka A, Aro EM (2011) The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J Proteome Res 10: 5338–5353 PubMed

Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. Culture of Marine Invertebrates Animals. Springer, New York, NY, pp 29–60

Gundermann K, Wagner V, Mittag M, Büchel C (2019) Fucoxanthin-chlorophyll protein complexes of the centric diatom Cyclotella Meneghiniana differ in Lhcx1 and Lhcx6_1 content. Plant Physiol 179: 1779–1795 PubMed PMC

Jäger S, Büchel C (2019) Cation-dependent changes in the thylakoid membrane appression of the diatom Thalassiosira pseudonana. Biochim Biophys Acta Bioenerg 1860: 41–51 PubMed

Järvi S, Suorsa M, Paakkarinen V, Aro EM (2011) Optimized native gel systems for separation of thylakoid protein complexes: Novel super- and mega-complexes. Biochem J 439: 207–214 PubMed

Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167: 191–194

Juhas M, Büchel C (2012) Properties of photosystem i antenna protein complexes of the diatom Cyclotella meneghiniana. J Exp Bot 63: 3673–3682 PubMed PMC

Kereïche S, Kouřil R, Oostergetel GT, Fusetti F, Boekema EJ, Doust AB, van der Weij-de Wit CD, Dekker JP (2008) Association of chlorophyll a/c2 complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24. Biochim Biophys Acta Bioenerg 1777: 1122–1128 PubMed

Kouřil R, Nosek L, Semchonok D, Boekema EJ, Ilík P (2018) Organization of plant photosystem II and photosystem I supercomplexes. Subcell Biochem 87: 259–286 PubMed

Kouřil R, Oostergetel GT, Boekema EJ (2011) Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochim Biophys Acta Bioenerg 1807: 368–374 PubMed

Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71–76 PubMed

De La Rosa-Trevín JM, Quintana A, Del Cano L, Zaldívar A, Foche I, Gutiérrez J, Gómez-Blanco J, Burguet-Castell J, Cuenca-Alba J, Abrishami V, et al. (2016) Scipion: A software framework toward integration, reproducibility and validation in 3D electron microscopy. J Struct Biol 195: 93–99 PubMed

Levitan O, Chen M, Kuang X, Cheong KY, Jiang J, Banal M, Nambiar N, Gorbunov MY, Ludtke SJ, Falkowski PG, et al. (2019) Structural and functional analyses of photosystem II in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA 116: 17316–17322 PubMed PMC

Lyumkis D (2019) Challenges and opportunities in cryo-EM single-particle analysis. J Biol Chem 294: 5181–5197 PubMed PMC

Marco P, Elman T, Yacoby I (2019) Binding of ferredoxin NADP+ oxidoreductase (FNR) to plant photosystem I. Biochim Biophys Acta Bioenerg 1860: 689–698 PubMed

Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36–51 PubMed

Nagao R, Takahashi S, Suzuki T, Dohmae N, Nakazato K, Tomo T (2013) Comparison of oligomeric states and polypeptide compositions of fucoxanthin chlorophyll a/c-binding protein complexes among various diatom species. Photosynth Res 117: 281–288 PubMed

Nagao R, Kato K, Suzuki T, Ifuku K, Uchiyama I, Kashino Y, Dohmae N, Akimoto S, Shen JR, Miyazaki N, et al. (2019) Structural basis for energy harvesting and dissipation in a diatom PSII–FCPII supercomplex. Nat Plants 5: 890–901 PubMed

Nagao R, Kato K, Ifuku K, Suzuki T, Kumazawa M, Uchiyama I, Kashino Y, Dohmae N, Akimoto S, Shen JR, et al. (2020a) Structural basis for assembly and function of a diatom photosystem I-light-harvesting supercomplex. Nat Commun 11: 2481. PubMed PMC

Nagao R, Ueno Y, Akimoto S, Shen JR (2020b) Effects of CO2 and temperature on photosynthetic performance in the diatom Chaetoceros gracilis. Photosynth Res 146: 189–195 PubMed

Papagiannakis E, Van Stokkum IHM, Fey H, Büchel C, Van Grondelle R (2005) Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynth Res 86: 241–250 PubMed

Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25: 1605–1612 PubMed

Pi X, Tian L, Dai HE, Qin X, Cheng L, Kuang T, Sui SF, Shen JR (2018) Unique organization of photosystem I–light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc Natl Acad Sci USA 17: 4423–4428 PubMed PMC

Pi X, Zhao S, Wang W, Liu D, Xu C, Han G, Kuang T, Sui SF, Shen JR (2019) The pigment-protein network of a diatom photosystem II–light-harvesting antenna supercomplex. Science 365: 463 PubMed

Pinnola A, Alboresi A, Nosek L, Semchonok DA, Rameez A, Trotta A, Barozzi F, Kouřil R, Dall’Osto L, Aro EM, et al. (2018) A LHCB9-dependent photosystem I megacomplex induced under low light in Physcomitrella patens. Nat Plants 4: 910–919 PubMed

Pyszniak AM, Gibbs SP (1992) Immunocytochemical localization of photosystem I and the fucoxanthin-chlorophyll a/c light-harvesting complex in the diatom Phaeodactylum tricornutum. Protoplasma 166: 208–217

Röding A, Boekema E, Büchel C (2018) The structure of FCPb, a light-harvesting complex in the diatom Cyclotella meneghiniana. Photosynth Res 135: 203–211 PubMed

Scheres SHW (2012) RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180: 519–530 PubMed PMC

Schober AF, Flori S, Finazzi G, Kroth PG, Bártulos CR (2018) Isolation of plastid fractions from the diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum.Methods Mol Biol 1829: 189–203 PubMed

Schober AF, Río Bártulos C, Bischoff A, Lepetit B, Gruber A, Kroth PG (2019) Organelle studies and proteome analyses of mitochondria and plastids fractions from the diatom Thalassiosira pseudonana. Plant Cell Physiol 60: 1811–1828 PubMed PMC

Su X, Wei X, Zhu D, Chang W, Liu Z, Zhang X, Li M, Ma J, Wei X, Cao P, et al. (2017) Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357: 815–820 PubMed

Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157: 38–46 PubMed

Wang W, Yu LJ, Xu C, Tomizaki T, Zhao S, Umena Y, Chen X, Qin X, Xin Y, Suga M, et al. (2019) Structural basis for blue-green light harvesting and energy dissipation in diatoms. Science 363: 598 PubMed

Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution. Nature 534: 69–74 PubMed

Westermann M, Rhiel E (2005) Localisation of fucoxanthin chlorophyll a/c-binding polypeptides of the centric diatom Cyclotella cryptica by immuno-electron microscopy. Protoplasma 225: 217–223 PubMed

Xu C, Pi X, Huang Y, Han G, Chen X, Qin X, Huang G, Zhao S, Yang Y, Kuang T, et al. (2020) Structural basis for energy transfer in a huge diatom PSI-FCPI supercomplex. Nat Commun 11: 5081. PubMed PMC

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