Abstract
Diatoms contribute about 20–25% to the global marine productivity and are successful autotrophic players in all aquatic ecosystems, which raises the question whether this performance is caused by differences in their photosynthetic apparatus. Photo-CIDNP MAS NMR presents a unique tool to obtain insights into the reaction centres of photosystems (PS), by selective enhancement of NMR signals from both, the electron donor and the primary electron acceptor molecules. Here, we present the first observation of the solid-state photo-CIDNP effect in the pennate diatoms. In comparison to plant PSs, similar spectral patterns have been observed for PS I at 9.4 T and PS II at 4.7 T in the PSs of Phaeodactylum tricornutum. Studies at different magnetic fields reveal a surprising sign change of the 13C photo-CIDNP MAS NMR signals indicating an alternative arrangement of cofactors which allows to quench the Chl a donor triplet state in contrast to the situation in plant PS II. This unusual quenching mechanism is related to a carotenoid molecule in close vicinity to the Chl a donor. In addition to the photo-CIDNP MAS NMR signals arising from the donor and the primary electron acceptor cofactors, a complete set of signals of the imidazole ring ligating to the magnesium of Chl a can be observed.
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Alia A, Matysik J, Soede-Huijbregts C et al (2001) Ultrahigh field MAS NMR dipolar correlation spectroscopy of the histidine residues in light-harvesting complex II from photosynthetic bacteria reveals partial internal charge transfer in the B850/His complex. J Am Chem Soc 123:4803–4809. https://doi.org/10.1021/ja002591z
Alia A, Roy E, Gast P et al (2004) Photochemically induced dynamic nuclear polarization in photosystem I of plants observed by 13C magic-angle spinning NMR. J Am Chem Soc 126:12819–12826. https://doi.org/10.1021/ja048051&%23x002B
Alia A, Wawrzyniak PK, Janssen GJ, et al. (2009) Differential charge polarization of axial histidines in bacterial reaction centers balances the asymmetry of the special pair. J Am Chem Soc 131:9626–9627. https://doi.org/10.1021/ja9028507
Allen JP, Williams JC (1998) Photosynthetic reaction centers. FEBS Lett 438:5–9. https://doi.org/10.1016/S0014-5793(98)01245-9
Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, Mc Crow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473:203–207. https://doi.org/10.1038/nature10074
Amunts A, Nelson N (2008) Functional organization of a plant Photosystem I: evolution of a highly efficient photochemical machine. Plant Physiol Biochem 46:228–237. https://doi.org/10.1016/j.plaphy.2007.12.013
Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447:58–63. https://doi.org/10.1038/nature05687
Armbrust EV (2009) The life of diatoms in the world´s oceans. Nature 459:185–189. https://doi.org/10.1038/nature08057
Armbrust EV, Berges JA, Bowler C et al (2004) The genome of the diatom thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86. https://doi.org/10.1126/science.1101156
Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34:619–631. https://doi.org/10.1042/BST0340619
Bennett AE, Rienstra CM, Auger M, Lakshmi KV, Griffin RG (1995) Heteronuclear decoupling in rotating solids. J Chem Phys 103:6951–6958. https://doi.org/10.1063/1.470372
Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635. https://doi.org/10.1038/nature02200
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2009) GenBank. Nucleic Acids Res 37(Database issue):D26–D31. https://doi.org/10.1093/nar/gkn723
Bielecki A, Burum DB (1995) Temperature-dependence of 207PB MAS spectra of solid lead nitrate: an accurate, sensitive thermometer for variable-temperature MAS. J Magn Reson 116:215–220
Bode B, Thamarath SS, Sai Sankar Gupta KB, Alia A, Jeschke G, Matysik J (2013) The solid-state photo-CIDNP effect and its analytical application. In: Kuhn L (ed) Hyperpolarization methods in NMR spectroscopy. Springer, New York, pp 105–121
Boender GJ (1996) Ph.D. Thesis, Dissertation, Univ. Leiden
Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244
Boxer SG, Closs GL, Katz JJ (1974) The effect of magnesium coordination on the 13C and 15N magnetic resonance spectra of chlorophyll a. Energies of nitrogen nπ* states as deduced from a the relative complete assignment of chemical shifts. J Am Chem Soc 96:7058–7066. https://doi.org/10.1021/ja00829a038
Bryant DA, Garcia Costas AM, Maresca JA et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526. https://doi.org/10.1126/science.1143236
Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev Camb Philos Soc 73:203–266. https://doi.org/10.1017/S0006323198005167
Céspedes-Camacho IF, Matysik J (2014) Spin in photosynthetic electron transport. In: Golbeck J, van der Est 7 (eds) The biophysics of photosynthesis. Springer, New York, pp 141–170
Daviso E, Jeschke G, Matysik J (2008) Photochemically induced dynamic nuclear polarization (Photo-CIDNP) magic-angle spinning NMR. In: Aartsma TJ, Matysik J (eds) Biophysical techniques in photosynthesis. Springer, Dordrecht, pp 385–399
Daviso E, Prakash S, Alia A et al (2009) The electronic structure of the primary electron donor of reaction centers of purple bacteria at the atomic resolution as observed by photo-CIDNP 13C MAS NMR. Proc Natl Acad Sci USA 106:22281–22286
Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39. https://doi.org/10.1016/j.bbabio.2004.09.009
Deligiannakis Y, Rutherford A (2001) Electron spin echo envelope modulation spectroscopy in photosystem I. Biochim Biophys Acta 1507, 226–246. https://doi.org/10.1016/S0005-2728(01)00201-8
Diller A, Alia A, Roy E et al (2005) Photo-CIDNP solid-state NMR on photosystems I and II: what makes P680 special? Photosynth Res 84:303–308. https://doi.org/10.1007/s11120-005-0411-0
Diller A, Roy E, Gast P et al (2007a) 15N photochemically induced dynamic nuclear polarization magic-angle spinning NMR analysis of the electron donor of photosystem II. Proc Natl Acad Sci USA 104:12767–12771. https://doi.org/10.1073/pnas.0701763104
Diller A, Prakash S, Alia A, Gast P, Matysik J, Jeschke G (2007b) Signals in solid-state photochemically induced dynamic nuclear polarization recover faster than with the longitudinal relaxation time. J Phys Chem B 111:10606–10614. https://doi.org/10.1021/jp072428r
Diller A, Alia A, Gast P et al (2008) 13C Photo-CIDNP MAS NMR on the LH1-RC Complex of Rhodopseudomonas acidophilia. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Energy from the sun. Springer, Dordrecht, pp 55–58
Dyballa N, Metzger S (2009) Fast and sensitive colloidal coomassie G-250 staining for proteins in polyacrylamide gels. J Vis Exp 30:1431. https://doi.org/10.3791/1431
Egorova-Zachernyuk TA, van Rossum B, Boender GJ et al (1997) Characterization of pheophytin ground states in rhodobacter sphaeroides R26 photosynthetic reaction centers from multispin pheophytin enrichment and 2-D 13C MAS NMR dipolar correlation spectroscopy. Biochemistry 36:7513–7519. https://doi.org/10.1021/bi962770m
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. https://doi.org/10.1126/science.1093087
Fischer MR, de Groot HJM, Raap J, Winkel C, Hoff AJ, Lugtenburg J (1992) Carbon-13 magic angle spinning NMR study of the light-induced and temperature-dependent changes in Rhodobacter sphaeroides R26 reaction centers enriched in [4′-13C]tyrosine. Biochemistry 31:11038–11049. https://doi.org/10.1021/bi00160a013
Flori S, Journeau P-H, Bailleul B et al (2017) Plastid thylakoid architecture optimizes photosynthesis in diatoms, Nat Commun 8:15885. https://doi.org/10.1038/ncomms15885
Gibbs SP (1962) The ultrastructure of the chloroplasts of algae. Ultrastruct Res 7:418–435. https://doi.org/10.1016/S0022-5320(62)90038-2
Gibbs SP (1970) The comparative ultrastructure of the algal chloroplast. Ann N Y Acad Sci 175:454–473
Goessling JW, Su Y, Cartaxana P et al (2018) Structure-based optics of centric diatom frustules: modulation of the in vivo light field for efficient diatom photosynthesis. New Phytol 219:122–134. https://doi.org/10.1111/nph.15149
Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32. https://doi.org/10.1016/j.jplph.2014.03.004
Gräsing D, Bielytskyi P, Céspedes-Camacho IF, Alia A, Marquardsen T, Engelke F, Matysik J (2017) Field-cycling NMR with high-resolution detection under magic-angle spinning: determination of field-window for nuclear hyperpolarization in a photosynthetic reaction center. Sci Rep 7:12111. https://doi.org/10.1038/s41598-017-10413-y
Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenetic photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 47:685–714. https://doi.org/10.1146/annurev.arplant.47.1.685
Grouneva I, Jakob T, Wilhelm C, Goss R. (2009) The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim Biophys Acta 1787:929–938
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342. https://doi.org/10.1038/nsmb.1559
Haynes WM (ed) (2015) CRC handbook of chemistry and physics. CRC Press, Boca Raton, pp 3–142
Janssen GJ (2013) The Heart of oxygenetic photosynthesis illuminated. Dissertation, Univ. Leiden
Janssen GJ, Daviso E, van Son M et al. (2010) Observation of the solid-state photo-CIDNP effect in entire cells of cyanobacteria Synechocystis. Photosynth Res 104:275–282. https://doi.org/10.1007/s11120-009-9508-1
Janssen GJ, Roy E, Matysik J, Alia A (2012) 15N photo-CIDNP MAS NMR to reveal functional heterogeneity in electron donor of different plant organisms. Appl Magn Reson 42:57–67. https://doi.org/10.1007/s00723-011-0283-8
Jensen PE, Bassi R, Boekema EJ et al (2007) Structure, function and regulation of plant photosystem I. Biochim Biophys Acta 1767:335–352. https://doi.org/10.1016/j.bbabio.2007.03.004
Jeschke G (1998) A new mechanism for chemically induced dynamic nuclear polarization in the solid state. J Am Chem Soc 120:4425–4429. https://doi.org/10.1021/ja973744u
Jeschke G, Matysik J (2003) A reassessment of the origin of photochemically induced dynamic nuclear polarization effects in solids. Chem Phys 294:239–255. https://doi.org/10.1016/S0301-0104(03)00278-7
Jordan P, Fromme P, Witt HAT et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. https://doi.org/10.1038/35082000
Käß H, Lubitz W (1996) Evaluation of 2D-ESEEM data of 15N-labeled radical cations of the primary donor P700 in photosystem I and chlorophyll a. Phys Lett 251:193–203
Kustka AB, Allen AE, Morel FMM (2007) Sequence analysis and transcriptional regulation of iron acquisition genes in two marine diatoms. J Phycol 43:715–729. https://doi.org/10.1111/j.1529-8817.2007.00359.x
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Lavaud J, Goss R (2014) In: Demmig-Adams B, Adams III WW, Garab G, Govindjee (eds) Non-photochemical quenching and thermal energy dissipation in plants, algae and cyanobacteria. Series: Advances in photosynthesis and respiration. Springer, Dordrecht
Lavaud J, van Gorkom HJ, Etienne A (2002), Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:51–59. https://doi.org/10.1023/A:1020890625141
Lepetit B (2010) Untersuchungen zur Struktur der Antennenkomplexe und zur Lokalisation der Xanthophyllzykluspigmente in Diatomeen, Dissertation, Universität Leipzig
Lepetit B, Volke D, Szabó M, Hoffmann R, Garab G, Wilhelm C, Goss R (2007) Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. Biochemistry 46:9813–9822. https://doi.org/10.1021/bi7008344
Li S, Hong M (2011) Protonation, tautomerization, and rotameric structure of histidine: a comprehensive study by magic-angle-spinning solid-state NMR. J Am Chem Soc 133:1534–1544. https://doi.org/10.1021/ja108943n
Loll B, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044. https://doi.org/10.1038/nature04224
Lommer M. Specht M, Roy A-S et al (2012) Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol 13:1–20. https://doi.org/10.1186/gb-2012-13-7-r66
Mac M, Tang X-S, Diner BA, McCracken J, Babcock GT (1996) Identification of histidine as an axial ligand to P700+. Biochemistry 35:13288–13293. https://doi.org/10.1021/bi961765f
Mann DG, Droop SJM (1996) Biodiversity, biogeography and conservation of diatoms. Hydrobiologia 336:19–32. https://doi.org/10.1007/BF00010816
Matysik J, Alia A, Hollander JG et al (2000) A set-up to study photochemically induced dynamic nuclear polarization in photosynthetic reaction centres by solid-state NMR. Indian J Biochem Biophys 37:418
Matysik J, Diller A, Roy E, Alia A (2009) The solid-state photo-CIDNP effect. Photosynth Res 102:427–435. https://doi.org/10.1007/s11120-009-9403-9
McDermott A, Zysmilich MG, Polenova T (1998) Solid state NMR studies of photoinduced polarization in photosynthetic reaction centers: mechanism and simulations. Solid State Nucl Magn Reson 11:21–47. https://doi.org/10.1016/S0926-2040(97)00094-5
Mock T, Otillar RP, Strauss J et al (2017) Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541:536–540. https://doi.org/10.1038/nature20803
Nagao R, Tomo T, Noguchi E, et al. (2009) Purification and characterization of a stable oxygen-evolving photosystem II complex from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1797:160–166. https://doi.org/10.1016/j.bbabio.2009.09.008
Nagao R, Suga M, Niikura A et al (2013) Crystal structure of Psb31, a novel extrinsic protein of PSII from a marine centric diatom and implications for ist binding and function. Biochemistry 52:6646–6652. https://doi.org/10.1021/bi400770d
Najdanova M, Janssen GJ, de Groot HJM et al (2015) Analysis of electron donors in photosystems in oxygenic photosynthesis by photo-CIDNP MAS NMR. J Photochem Photobiol B 152:261–271. https://doi.org/10.1016/j.jphotobiol.2015.08.001
Polenova T, McDermott AE (1999) A coherent mixing mechanism explains the photoinduced nuclear polarization in photosynthetic reaction centers. J Phys Chem 103:535–548. https://doi.org/10.1021/jp9822642
Prakash S, Alia A, Gast P, de Groot HJM, Jeschke G, Matysik J (2005a) Magnetic field dependence of photo-CIDNP MAS NMR on photosynthetic reaction centres of Rhodobacter sphaeroides WT. J Am Chem Soc 127:14290–14298
Prakash S, Tong SH, Alia A, Gast P, de Groot HJM, Jeschke G, Matysik J (2005b) 15N photo-CIDNP MAS NMR on reaction centers of Rhodobacter sphaeroides. In: van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects to global perspektives. Allen Press, Montreal, pp 236–238
Prakash S, Alia A, Gast P et al. (2006) Photo-CIDNP MAS NMR in intact cells of Rhodobacter sphaeroides R26: molecular and atomic resolution at nanomolar concentration. J Am Chem Soc 128:12794–12799. https://doi.org/10.1021/ja0623616
Pyszniak AM, Gibbs SP (1992) Immunocytochemical localization of photosystem I and the fucoxanthin-chlorophylla/c light-harvesting complex in the diatom Phaeodactylum tricornutum. Protoplasma 166:208–218. https://doi.org/10.1007/BF01322783
Roy E, Diller A, Alia A et al. (2007a) Magnetic field dependence of 13C photo-CIDNP MAS NMR in plant photosystems I and II. Appl Magn Reson 31:193–204. https://doi.org/10.1007/BF03166256
Roy E, Alia A, Gast P et al. (2007b) Photochemically induced dynamic nuclear polarization in the reaction center of the green sulphur bacterium Chlorobium tepidum observed by 13C MAS NMR. Biochim Biophys Acta 1767:610–615. https://doi.org/10.1016/j.bbabio.2006.12.012
Roy E, Rohmer T, Gast P et al (2008) Characterization of the primary radical pair in reaction centers of Heliobacillus mobilis by 13C Photo-CIDNP MAS NMR. Biochemistry 47:4629–4635. https://doi.org/10.1021/bi800030g
Sayers EW, Barrett T, Benson DA et al. (2009) Database resources of the National Center for biotechnology information. Nucleic Acids Res. https://doi.org/10.1093/nar/gkn741
Schubert WD, Klukas O, Saenger W et al (1998) A common ancestor for oxygenetic and anoxygenetic photosynthetic systems: a comparison based on the structural model of photosystem I. J Mol Biol 280:297–314. https://doi.org/10.1006/jmbi.1998.1824SDBS
Sétif P, Brettel K (1990) Photosystem I photochemistry under highly reducing conditions: study of the P700 triplet state formation from the secondary radical pair (P700 + – A – 1). Biochim Biophys Acta 1020:232–238. https://doi.org/10.1016/0005-2728(90)90152-T
Shuvalov VA, Parson WW (1981) Energies and kinetics of radical pairs involving bacteriochlorophyll and bacteriopheophytin in bacterial reaction centers. Proc Natl Acad Sci USA 78:957–961
Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32. https://doi.org/10.1016/S1434-4610(99)70006-4
Smetacek V (2000) Oceanography: the giant diatom dump. Nature 406:574–575. https://doi.org/10.1038/35020665
Sosnovsky D, Jeschke G, Matysik J et al (2016) Level crossing analysis of chemically induced dynamic nuclear polarization: towards a common description of liquid-state and solid-state cases. J Chem Phys 144:144202. https://doi.org/10.1063/1.4945341
Spectral Database for Organic Compounds (1999) National Institute of Advanced Industrial Science and Technology, NMR: K. Haya-mizu, M. Yanagisawa, O. Yamamoto, MS: N. Wasada, ESR: K. Someno, IR: K. Tanabe, T. Tamura, Raman: K. Tanabe, J. Hiraishi, 13C NMR spectrum; SDBS No.: 1188 CDS-07-029, http://sdbs.db.aist.go.jp/sdbs/cgi-bin/direct_frame_top.cgi. Accessed January 20, 2017
Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692. https://doi.org/10.1038/nature02954
Sumper M, Brunner E (2008) Silica biomineralisation in diatoms: the model organism Thalassiosira pseudonana. ChemBioChem 9:1187–1194. https://doi.org/10.1002/cbic.2007007764
Thamarath SS, Heberle J, Hore P et al (2010) Solid-state photo-CIDNP effect observed in phototropin LOV1-C57S by 13C magic-angle spinning NMR spectroscopy. J Am Chem Soc 132:15542–15543. https://doi.org/10.1021/ja1082969
Thamarath SS, Bode BE, Prakash S (2012) Electron spin density distribution in the special pair triplet of Rhodobacter sphaeroides R26 revealed by magnetic field dependence of the solid-state photo-CIDNP effect. J Am Chem Soc 134:5921–5930. https://doi.org/10.1021/ja2117377
Tréguer P, Nelson DM, van Bennekom AJ et al (1995) The silica balance in the world ocean: a reestimate. Science 268:375–379. https://doi.org/10.1126/science.268.5209.375
Wagner H, Jakob T, Lavaud J, Wilhelm C (2016) Photosystem II cycle activity and alternative electron transport in the diatom Phaeodactylum tricornutum under dynamic light conditions and nitrogen limitation. Photosynth Res 128:151–161. https://doi.org/10.1007/s11120-015-0209-7
Wei XP, Zhang XZ, Su XD, et al (2016) Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution. Nature 534:69–74. https://doi.org/10.1038/nature18020
Werner D (ed) (1977) The biology of the diatoms. Blackwell Scientific Publikations, Oxford, p 2
Wilhelm C, Büchel C, Fisahn J, Goss R, Jakob T, LaRoche J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG, (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124. https://doi.org/10.1016/j.protis.2006.02.003
Wisser D, Brückner SI, Wisser FM, Althoff-Ospelt G, Kaskel S, Brunner E (2015) (1)H-(13)C-(29)Si triple resonance and REDOR solid-state NMR-A tool to study interactions between biosilica and organic molecules in diatom cell walls. Solid State Nucl Magn Reson 66/67:33–39. https://doi.org/10.1016/j.ssnmr.2014.12.007
Zill JC (2017a) Der Festkörper photo-CIDNP-Effekt im Baum des Lebens. Dissertation, Universität Leipzig
Zill JC, Kansy M, Goss R et al (2017b) Photo-CIDNP in the reaction center of the datom Cyclotella meneghiniana observed by 13C MAS NMR. Z Phys Chem 231:347–367. https://doi.org/10.1515/zpch-2016-0806
Zysmilich MG, McDermott A (1994) Photochemically induced dynamic nuclear polarization in the solid-state 15N spectra of reaction centers from photosynthetic bacteria Rhodobacter sphaeroides R-26. J Am Chem Soc 116:8362–8363. https://doi.org/10.1021/ja00097a052
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The authors want to thank Dr. Matthias Findeisen for technical support.
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This study was funded by the Deutsche Forschungsgemeinschaft DFG (MA4972/2-1).
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Zill, J.C., Kansy, M., Goss, R. et al. 15N photo-CIDNP MAS NMR on both photosystems and magnetic field-dependent 13C photo-CIDNP MAS NMR in photosystem II of the diatom Phaeodactylum tricornutum. Photosynth Res 140, 151–171 (2019). https://doi.org/10.1007/s11120-018-0578-9
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DOI: https://doi.org/10.1007/s11120-018-0578-9