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Modular antenna of photosystem I in secondary plastids of red algal origin: a Nannochloropsis oceanica case study

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Abstract

Photosystem I (PSI) is a multi-subunit integral pigment–protein complex that performs light-driven electron transfer from plastocyanin to ferredoxin in the thylakoid membrane of oxygenic photoautotrophs. In order to achieve the optimal photosynthetic performance under ambient irradiance, the absorption cross section of PSI is extended by means of peripheral antenna complexes. In eukaryotes, this role is played mostly by the pigment–protein complexes of the LHC family. The structure of the PSI-antenna supercomplexes has been relatively well understood in organisms harboring the primary plastid: red algae, green algae and plants. The secondary endosymbiotic algae, despite their major ecological importance, have so far received less attention. Here we report a detailed structural analysis of the antenna-PSI association in the stramenopile alga Nannochloropsis oceanica (Eustigmatophyceae). Several types of PSI-antenna assemblies are identified allowing for identification of antenna docking sites on the PSI core. Instances of departure of the stramenopile system from the red algal model of PSI-Lhcr structure are recorded, and evolutionary implications of these observations are discussed.

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Abbreviations

Chl:

Chlorophyll

N. :

Nannochloropsis

P700:

The primary donor of the photosystem I reaction center

PS:

Photosystem

PMS:

Phenazine methosulfate

RC:

Reaction center

IsiA:

Outer antenna of PSI in cyanobacteria

Pcb:

Outer antenna of PSI in chlorophyll b-containing cyanobacteria

References

  • Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447:58

    Article  CAS  PubMed  Google Scholar 

  • Basso S, Simionato D, Gerotto C, Segalla A, Giacometti GM, Morosinotto T (2014) Characterization of the photosynthetic apparatus of the Eustigmatophycean Nannochloropsis gaditana: evidence of convergent evolution in the supramolecular organization of photosystem I. Biochim Biophys Acta 1837:306–314

    Article  CAS  PubMed  Google Scholar 

  • Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745

    Article  CAS  PubMed  Google Scholar 

  • Bibby TS, Mary I, Nield J, Partensky F, Barber J (2003) Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature 424:1051–1054

    Article  CAS  PubMed  Google Scholar 

  • Bína D, Litvín R, Vacha F, Siffel P (2006) New multichannel kinetic spectrophotometer–fluorimeter with pulsed measuring beam for photosynthesis research. Photosynth Res 88:351–356

    Article  PubMed  Google Scholar 

  • Bína D, Gardian Z, Herbstová M, Kotabová E, Koník P, Litvín R, Prášil O, Tichý J, Vácha F (2014) Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. II. Biochemistry and spectroscopy. Biochim Biophys Acta 1837:802–810

    Article  PubMed  Google Scholar 

  • Bína D, Herbstová M, Gardian Z, Vácha F, Litvín R (2016) Novel structural aspect of the diatom thylakoid membrane: lateral segregation of photosystem I under red-enhanced illumination. Sci Rep 6:25583

    Article  PubMed  PubMed Central  Google Scholar 

  • Boekema EJ, Dekker JP, Vanheel MG, Rogner M, Saenger W, Witt I, Witt HT (1987) Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 217:283–286

    Article  CAS  Google Scholar 

  • Boekema EJ, Wynn RM, Malkin R (1990) The structure of spinach photosystem I studied by electron microscopy. Biochim Biophys Acta 1017:49–56

    Article  CAS  Google Scholar 

  • Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J, Rogner M (1995) Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92:175–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001a) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748

    Article  CAS  PubMed  Google Scholar 

  • Boekema EJ, Jensen PE, Schlodder E, van Breemen JFL, van Roon H, Scheller HV, Dekker JP (2001b) Green plant photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry 40:1029–1036

    Article  CAS  PubMed  Google Scholar 

  • Büchel C, Wilhelm C (1993) Isolation and characterization of a photosystem I-associated antenna (LHC I) and a photosystem I-core complex from the chlorophyll c-containing alga Pleurochloris meiringensis (Xanthophyceae). J Photochem Photobiol B Biol 20:87–93

    Article  Google Scholar 

  • Büchel C, Wilhelm C, Hauswirth N, Wild A (1992) Evidence for a lateral heterogeneity by patch-work like areas enriched in photosystem I complexes in the three thylakoid lamellae of Pleurochloris meiringensis (Xanthophyceae). J Crypt Bot 2:375–386

    Google Scholar 

  • Bumba L, Prášil O, Vácha F (2005) Antenna ring around trimeric photosystem I in chlorophyll b containing cyanobacterium Prochlorothrix hollandica. Biochim Biophys Acta 1708:1–5

    Article  CAS  PubMed  Google Scholar 

  • Busch A, Hippler M (2011) The structure and function of eukaryotic photosystem I. Biochim Biophys Acta 1807:864–877

    Article  CAS  PubMed  Google Scholar 

  • Busch A, Nield J, Hippler M (2010) The composition and structure of photosystem I-associated antenna from Cyanidioschyzon merolae. Plant J 62:886–897

    Article  CAS  PubMed  Google Scholar 

  • Busch A, Petersen J, Webber-Birungi M-T, Powikrowska M, Lassen LMM, Naumann-Busch B, Nielsen AZ, Ye J, Boekema EJ, Jensen ON, Lunde C, Jensen PE (2013) Composition and structure of photosystem I in the moss Physcomitrella patens. J Exp Bot 64:2689–2699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de la Rosa-Trevín JM, Otón J, Marabini R, Zaldívar A, Vargas J, Carazo JM, Sorzano COS (2013) Xmipp 3.0: an improved software suite for image processing in electron microscopy. J Struct Biol 184:321–328

    Article  PubMed  Google Scholar 

  • Dittami SM, Michel G, Collén J, Boyen C, Tonon T (2010) Chlorophyll-binding proteins revisited—a multigenic family of light-harvesting and stress proteins from a brown algal perspective. BMC Evol Biol 10:365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drop B, Webber-Birungi M, Fusetti F, Kouřil R, Redding KE, Boekema EJ, Croce R (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286:44878–44887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drop B, Yadav SKN, Boekema EJ, Croce R (2014a) Consequences of state transitions on the structural and functional organization of photosystem I in the green alga Chlamydomonas reinhardtii. Plant J 78:181–191

    Article  CAS  PubMed  Google Scholar 

  • Drop B, Webber-Birungi M, Yadav SKN, Filipowicz-Szymanska A, Fusetti F, Boekema EJ, Croce R (2014b) Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim Biophys Acta 1837:63–72

    Article  CAS  PubMed  Google Scholar 

  • Gantt E, Grabowski B, Cunningham FX (2003) Antenna systems of red algae: phycobilisomes with photosystem II and chlorophyll complexes with photosystem I. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer, Dordrecht, pp 307–322

    Chapter  Google Scholar 

  • Gardian Z, Bumba L, Schrofel A, Herbstová M, Nebesářová J, Vácha F (2007) Organisation of photosystem I and photosystem II in red alga Cyanidium caldarium: encounter of cyanobacterial and higher plant concepts. Biochim Biophys Acta 1767:725–731

    Article  CAS  PubMed  Google Scholar 

  • Gardian Z, Tichý J, Vácha F (2011) Structure of PSI, PSII and antennae complexes from yellow-green alga Xanthonema debile. Photosynth Res 108:25–32

    Article  CAS  PubMed  Google Scholar 

  • Germano M, Yakushevska AE, Keegstra W, van Gorkom HJ, Dekker JP, Boekema EJ (2002) Supramolecular organization of photosystem I and light-harvesting complex I in Chlamydomonas reinhardtii. FEBS Lett 525:121–125

    Article  CAS  PubMed  Google Scholar 

  • Grouneva I, Rokka A, Aro E-M (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

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Herbstová M, Bína D, Koník P, Gardian Z, Vácha F, Litvín R (2015) Molecular basis of chromatic adaptation in pennate diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1847:534–543

    Article  PubMed  Google Scholar 

  • Ikeda Y, Yamagishi A, Komura M, Suzuki T, Dohmae N, Shibata Y, Itoh S, Koike H, Satoh K (2013) Two types of fucoxanthin-chlorophyll-binding proteins I tightly bound to the photosystem I core complex in marine centric diatoms. Biochim Biophys Acta 1827:529–539

    Article  CAS  PubMed  Google Scholar 

  • Kargul J, Nield J, Barber J (2003) Three-dimensional reconstruction of a light-harvesting complex I photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii. J Biol Chem 278:16135–16141

    Article  CAS  PubMed  Google Scholar 

  • Keşan G, Litvín R, Bína D, Durchan M, Šlouf V, Polívka T (2016) Efficient light-harvesting using non-carbonyl carotenoids: energy transfer dynamics in the VCP complex from Nannochloropsis oceanica. Biochim Biophys Acta 1857:370

    Article  PubMed  Google Scholar 

  • Komenda J, Knoppová J, Kopečná J, Sobotka R, Halada P, Yu J, Nickelsen J, Boehm M, Nixon PJ (2012a) The Psb27 assembly factor binds to the CP43 complex of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 158:476–486

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Sobotka R, Nixon PJ (2012b) Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251

    Article  CAS  PubMed  Google Scholar 

  • Kotabová E, Jarešová J, Kaňa R, Sobotka R, Bína D, Prášil O (2014) Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim Biophys Acta 1837:734–743

    Article  PubMed  Google Scholar 

  • Kouřil R, Arteni AA, Lax J, Yeremenko N, D’Haene S, Rögner M, Matthijs HCP, Dekker JP, Boekema EJ (2005a) Structure and functional role of supercomplexes of IsiA and photosystem I in cyanobacterial photosynthesis. FEBS Lett 579:3253–3257

    Article  PubMed  Google Scholar 

  • Kouřil R, van Oosterwijk N, Yakushevska AE, Boekema EJ (2005b) Photosystem I: a search for green plant trimers. Photochem Photobiol Sci 4:1091–1094

    Article  PubMed  Google Scholar 

  • Kouřil R, Zygadlo A, Arteni AA, de Wit CD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005c) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 33:10935–10940

    Google Scholar 

  • Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2–12

    Article  PubMed  Google Scholar 

  • Kouřil R, Nosek L, Bartoš J, Boekema EJ, Ilík P (2016) Evolutionary loss of light-harvesting proteins Lhcb6 and Lhcb3 in major land plant groups—break-up of current dogma. New Phytol 210:808–814

    Article  PubMed  Google Scholar 

  • Li M, Semchonok DA, Boekema EJ, Bruce BD (2014) Characterization and evolution of tetrameric photosystem I from the thermophilic cyanobacterium Chroococcidiopsis sp. TS-821. Plant Cell 26:1230–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Litvín R, Bína D, Herbstová M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130(1):137–150

    Article  PubMed  Google Scholar 

  • Lucinski R, Schmid VHR, Jansson S, Klimmek F (2006) Lhca5 interaction with plant photosystem I. FEBS Lett 580:6485–6488

    Article  CAS  PubMed  Google Scholar 

  • Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 Å resolution. eLife 4:e07433

    Article  PubMed  PubMed Central  Google Scholar 

  • Neilson JAD, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71

    Article  CAS  PubMed  Google Scholar 

  • Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan H, Šlapeta J, Carter D, Chen M (2012) Phylogenetic analysis of the light-harvesting system in Chromera velia. Photosynth Res 111(1–2):19–28

    Article  CAS  PubMed  Google Scholar 

  • Qin X, Suga M, Kuang T, Shen JR (2015) Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348:989–995

    Article  CAS  PubMed  Google Scholar 

  • Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheres SHW (2012b) A Bayesian view on cryo-EM structure determination. J Mol Biol 415:406–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ševčíková T, Horák A, Klimeš V, Zbránková V, Demir-Hilton E, Sudek S, Jenkins J, Schmutz J, Přibyl P, Fousek J, Vlček Č, Lang BF, Oborník M, Worden AZ, Eliáš M (2015) Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci Rep 5:10134

    Article  PubMed  PubMed Central  Google Scholar 

  • Takahashi T, Inoue-Kashino N, Ozawa S-I, Takahashi Y, Kashino Y, Satoh K (2009) Photosystem II complex in vivo is a monomer. J Biol Chem 284:15598–15606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thangaraj B, Jolley CC, Sarrou I, Bultema JB, Greyslak J, Whitelegge JP, Lin S, Kouřil R, Subramanyam R, Boekema EJ, Fromme P (2011) Efficient light harvesting in a dark, hot, acidic environment: the structure and function of PSI-LHCI from Galdieria sulphuraria. Biophys J 100:135–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tichý J, Gardian Z, Bína D, Koník P, Litvín R, Herbstová M, Pain A, Vácha F (2013) Light harvesting complexes of Chromera velia, photosynthetic relative of apicomplexan parasites. Biochim Biophys Acta 1827:723–729

    Article  PubMed  Google Scholar 

  • Veith T, Büchel C (2007) The monomeric photosystem I-complex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes. Biochim Biophys Acta 1767:1428–1435

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Iwai M, Narikawa R, Ikeuchi M (2009) Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol 50:1674–1680

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, Oostergetel GT, Jansson S, Boekema EJ, Croce R (2009) The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J Biol Chem 284:7803–7810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon HS, Muller KM, Sheath RG, Ott FD, Bhattacharya D (2006) Defining the major lineages of red algae (Rhodophyta). J Phycol 42:482–492

    Article  CAS  Google Scholar 

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Acknowledgments

This work was financially supported by the Czech Science Foundation Grant No. 14-01377P and by institutional funding RVO:60077344. Expert technical assistance of Ivana Hunalová and František Matoušek is gratefully acknowledged.

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    Authors and Affiliations

    1. Institute of Plant Molecular Biology, Biology Centre CAS, Branišovská 31, 370 05, České Budějovice, Czech Republic

      David Bína, Zdenko Gardian, Miroslava Herbstová & Radek Litvín

    2. Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05, České Budějovice, Czech Republic

      David Bína, Zdenko Gardian, Miroslava Herbstová & Radek Litvín

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    1. David Bína
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    Correspondence to Radek Litvín.

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    David Bína and Zdenko Gardian have contributed equally to the present work.

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    Bína, D., Gardian, Z., Herbstová, M. et al. Modular antenna of photosystem I in secondary plastids of red algal origin: a Nannochloropsis oceanica case study. Photosynth Res 131, 255–266 (2017). https://doi.org/10.1007/s11120-016-0315-1

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