Thylakoid Ultrastructure: Visualizing the Photosynthetic Machinery

  • Janina Steinbeck
  • Megan L. O’Mara
  • Ian L. Ross
  • Henning Stahlberg
  • Ben HankamerEmail author
Part of the Microbiology Monographs book series (MICROMONO, volume 31)


The surface of our planet receives ∼3020 ZJ per year of solar energy annually, which is >5000 times the energy required to power our entire global economy (∼0.6 ZJ per year). Of this energy, ∼43% is photosynthetic active light radiation (PAR) that can be used to drive microalgal biotechnologies for the production of food, fuels, high value products, carbon sequestration, and bioremediation. The first step of all light-driven microalgal processes is light capture. A diverse array of highly efficient, self-assembling, light-responsive “solar interfaces,” the thylakoid membranes, have evolved to tap into this abundant, but constantly changing, energy resource to power the biosphere. The photosynthetic machinery within the thylakoids is intricately arranged in a complex 3D architecture and designed to adapt dynamically (i.e., 4D: representing changes in 3D structures over time) to constantly changing environmental conditions, to maximize solar to chemical energy conversion. The ATP and NADPH generated are used to produce the complex set of biomolecules that collectively form biomass. Here, we review the structural organization of these amazing photosynthetic interfaces in the model organism Chlamydomonas reinhardtii and summarize recent advances in structural biology, which underpin the development of next-generation atomic resolution dynamic simulations of these systems. Revealing such a 4D atlas of 3D structures in atomic resolution detail is of fundamental importance to enable structure-guided design of natural photosynthetic systems for biotechnological application and to provide a blueprint for the design of nanoscale components, which are the building blocks for the development of next-generation artificial solar fuel systems.



The authors thank Olivier Vallon, Jacqueline Olive, Michel Recouvreur, Francis-André Wollman, Rosalba Rothnangel, and Rick Webb for the provision of EM images included in the figures. JS, IR, BH, and HS thank the Australian Research Council for financial support (DP130100346 and DP160101018).


  1. Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628PubMedCrossRefGoogle Scholar
  2. Adrian M, Dubochet J, Lepault J, McDowall AW (1984) Cryo-electron microscopy of viruses. Nature 308:32–36PubMedCrossRefGoogle Scholar
  3. Ago H, Adachi H, Umena Y, Tashiro T, Kawakami K, Kamiya N, Tian L, Han G, Kuang T, Liu Z, Wang F, Zou H, Enami I, Miyano M, Shen J-R (2016) Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J Biol Chem 291:5676–5687. doi: 10.1074/jbc.M115.711689 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alber F, Förster F, Korkin D, Topf M, Sali A (2008) Integrating diverse data for structure determination of macromolecular assemblies. Annu Rev Biochem 77:443–477PubMedCrossRefGoogle Scholar
  5. Ali RA, Landsberg MJ, Knauth E, Morgan GP, Marsh BJ, Hankamer B (2012) A 3D image filter for parameter-free segmentation of macromolecular structures from electron tomograms. PLoS One 7:e33697PubMedPubMedCentralCrossRefGoogle Scholar
  6. Allegretti M, Klusch N, Mills DJ, Vonck J, Kühlbrandt W, Davies KM (2015) Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase. Nature 521:237–240PubMedCrossRefGoogle Scholar
  7. Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291:25–29CrossRefGoogle Scholar
  8. Alric J (2014) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (II) involvement of the PGR5–PGRL1 pathway under anaerobic conditions. Biochem Biophys Acta 1897:825–834Google Scholar
  9. Alric J, Lavergne J, Rappaport F (2010) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions. Biochim Biophys Acta 1797:44–51PubMedCrossRefGoogle Scholar
  10. Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 A resolution. Nature 447:58–63PubMedCrossRefGoogle Scholar
  11. Amunts A, Toporik H, Borovikova A, Nelson N (2010) Structure determination and improved model of plant photosystem I. J Biol Chem 285:3478–3486PubMedCrossRefGoogle Scholar
  12. Amunts A, Brown A, Bai X, Llácer JL, Ramakrishnan TH, Emsley P, Long F, Murshudov G, SHW S, Ramakrishnan V (2014) Structure of the yeast mitochondrial large ribosomal subunit. Science 343:1485–1489PubMedPubMedCentralCrossRefGoogle Scholar
  13. Andoh Y, Yoshii N, Yamada A, Fujimoto K, Kojima H, Mizutani K, Nakagawa A, Nomoto A, Okazaki S (2014) All-atom molecular dynamics calculation study of entire poliovirus empty capsids in solution. J Chem Phys 141:1–11CrossRefGoogle Scholar
  14. Anthony KC, You C, Piehler J, Pomeranz Krummel DA (2014) High-affinity gold nanoparticle pin to label and localize histidine-tagged protein in macromolecular assemblies. Structure 22:628–635PubMedPubMedCentralCrossRefGoogle Scholar
  15. Asano S, Fukuda Y, Beck F, Aufderheide A, Förster F, Danev R, Baumeister W (2015) A molecular census of 26. Science 347:439–443PubMedCrossRefGoogle Scholar
  16. Austin JR, Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol 155:1601–1611PubMedPubMedCentralCrossRefGoogle Scholar
  17. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76:1052–1071Google Scholar
  18. Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA (2008) Structure–function of the cytochrome b6f complex. Photochem Photobiol 84:1349–1358PubMedCrossRefGoogle Scholar
  19. Barber J, Chow WS (1979) A mechanism for controlling the stacking and unstacking of chloroplast thylakoid membranes. FEBS Lett 105:5–10CrossRefGoogle Scholar
  20. Bassi R, Soen SY, Frank G, Zuber H, Rochaix JD (1992) Characterization of chlorophyll a/b proteins of photosystem I from Chlamydomonas reinhardtii. J Biol Chem 267:25714–25721PubMedGoogle Scholar
  21. Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635PubMedCrossRefGoogle Scholar
  22. Berger O, Edholm O, Jahnig F (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72:2002–2013PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bergner SV, Scholz M, Trompelt K, Barth J, Gäbelein P, Steinbeck J, Xue H, Clowez S, Fucile G, Goldschmidt-Clermont M, Fufezan C, Hippler M (2015) State transition7-dependent phosphorylation is modulated by changing environmental conditions and its absence triggers remodeling of photosynthetic protein complexes. Plant Physiol 168(2):615–634. doi: 10.1104/pp.15.00072 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Bes MT, Parisini E, Inda LA, Peleato ML, Saraiva L (1999) Crystal structure determination at 1.4 Å resolution of ferredoxin from the green alga Chlorella fusca. Structure 7:1201–1211PubMedCrossRefGoogle Scholar
  25. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–1645PubMedCrossRefGoogle Scholar
  26. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745PubMedCrossRefGoogle Scholar
  27. Biesiadka J, Loll B, Kern J, Irrgang K-D, Zouni A (2004) Crystal structure of cyanobacterial photosystem II at 3.2 Å resolution: a closer look at the Mn-cluster. Phys Chem Chem Phys 6:4733–4736CrossRefGoogle Scholar
  28. Binda C, Coda A, Aliverti A, Zanetti G, Mattevi A (1998) Structure of the mutant E92K of [2Fe-2S] ferredoxin I from Spinacia oleracea at 1.7 Å resolution. Acta Crystallogr D Biol Crystallogr 54:1353–1358PubMedCrossRefGoogle Scholar
  29. Boekema EJ, Dekker JP, van Heel MG, Rögner 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 217:283–286CrossRefGoogle Scholar
  30. Bovi D, Narzi D, Guidoni L (2014) Magnetic interactions in the catalyst used by nature to split water: a DFT + U multiscale study on the Mn4CaO5 core in photosystem II. New J Phys 16:015020CrossRefGoogle Scholar
  31. Bowler MW, Montgomery MG, Leslie AGW, Walker JE (2007) Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 Å resolution. J Biol Chem 282:14238–14242PubMedCrossRefGoogle Scholar
  32. Boyer PD (1997) The ATP synthase - a splendid molecular machine. Annu Rev Biochem 66:717–749PubMedCrossRefGoogle Scholar
  33. Boynton JE, Gillham NW, Chabot JF (1972) Chloroplast ribosome deficient mutants in the green alga Chlamydomonas reinhardi and the question of chloroplast ribosome function. J Cell Sci 10:267–305PubMedGoogle Scholar
  34. British Petroleum (2015) BP statistical review of world energy. June 2010:48Google Scholar
  35. Brumfeld V, Charuvi D, Nevo R, Chuartzman S, Tsabari O, Ohad I, Shimoni E, Reich Z (2008) A note on three-dimensional models of higher-plant thylakoid networks. Plant Cell Online 20:2546–2549CrossRefGoogle Scholar
  36. Büchel C, Kühlbrandt W (2005) Structural differences in the inner part of photosystem II between higher plants and cyanobacteria. Photosynth Res 85:3–13PubMedCrossRefGoogle Scholar
  37. Canny J (1986) A computational approach to edge detection. IEEE 8:679–698Google Scholar
  38. Carpenter EP, Beis K, Cameron AD, Iwata S (2008) Overcoming the challenges of membrane protein crystallography. Curr Opin Struct Biol 18:581–586PubMedPubMedCentralCrossRefGoogle Scholar
  39. Castaño-Díez D, Kudryashev M, Arheit M, Stahlberg H (2012) Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J Struct Biol 178:139–151PubMedCrossRefGoogle Scholar
  40. Catarious DM, Baydush AH, Floyd CE (2006) Characterization of difference of Gaussian filters in the detection of mammographic regions. Med Phys 33:4104–4114PubMedCrossRefGoogle Scholar
  41. Central Intelligence Agency (2017) The world factbook.…
  42. Chari A, Haselbach D, Kirves J-M, Ohmer J, Paknia E, Fischer N, Ganichkin O, Möller V, Frye JJ, Petzold G, Jarvis M, Tietzel M, Grimm C, Peters J-M, Schulman BA, Tittmann K, Markl J, Fischer U, Stark H (2015) ProteoPlex: stability optimization of macromolecular complexes by sparse-matrix screening of chemical space. Nat Methods 12:859–865PubMedPubMedCentralCrossRefGoogle Scholar
  43. Chen B-C, Legant WR, Wang K, Shao L, Milkie DE, Davidson MW, Janetopoulos C, Wu XS, Hammer JA, Liu Z, English BP, Mimori-Kiyosue Y, Romero DP, Ritter AT, Lippincott-Schwartz J, Fritz-Laylin L, Mullins RD, Mitchell DM, Bembenek JN, Reymann A-C, Bohme R, Grill SW, Wang JT, Seydoux G, Tulu US, Kiehart DP, Betzig E (2014) Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346:1257998PubMedPubMedCentralCrossRefGoogle Scholar
  44. Chuartzman SG, Nevo R, Shimoni E, Charuvi D, Kiss V, Ohad I, Brumfeld V, Reich Z (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20:1029–1039PubMedPubMedCentralCrossRefGoogle Scholar
  45. Cingolani G, Duncan TM (2011) Structure of the ATP synthase catalytic complex (F(1)) from Escherichia coli in an autoinhibited conformation. Nat Struct Mol Biol 18:701–707PubMedPubMedCentralCrossRefGoogle Scholar
  46. Cope J, Gilbert S, Rayment I, Mastronarde D, Hoenger A (2011) Cryo-electron tomography of microtubule-kinesin motor complexes. J Struct Biol 170:257–265CrossRefGoogle Scholar
  47. Cortese K, Vicidomini G, Gagliani MC, Boccacci P, Diaspro A, Tacchetti C (2013) High data output method for 3-D correlative light-electron microscopy using ultrathin cryosections. In: Suosa AA, Kruhlak MJ (eds) Nanoimaging. Springer, New York, pp 417–438CrossRefGoogle Scholar
  48. Danev R, Baumeister W (2016) Cryo-EM single particle analysis with the Volta phase plate. Elife. doi: 10.7554/eLife.13046.001
  49. Danev R, Buijsse B, Khoshouei M, Plitzko JM, Baumeister W (2014) Volta potential phase plate for in-focus phase contrast transmission electron microscopy. Proc Natl Acad Sci U S A 111:15635–15640PubMedPubMedCentralCrossRefGoogle Scholar
  50. Davies KM, Strauss M, Daum B, Kief JH, Osiewacz HD, Rycovska A, Zickermann V, Kuhlbrandt W (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc Natl Acad Sci 108:14121–14126PubMedPubMedCentralCrossRefGoogle Scholar
  51. de Boer P, Hoogenboom JP, Giepmans BNG (2015) Correlated light and electron microscopy: ultrastructure lights up! Nat Methods 12:503–513PubMedCrossRefGoogle Scholar
  52. de Castro IF, Sanz-Sánchez L, Risco C (2014) Chap 3: Metallothioneins for correlative light and electron microscopy (pp 55–70). In: Thomas M-R, Paul V (eds) Correlative light and electron microscopy II, Methods in cell biology, vol 124. Academic Press, Cambridge, 452 pp. isbn:978-0128010754Google Scholar
  53. Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3A resolution. Nature 318:618–624PubMedCrossRefGoogle Scholar
  54. Delosme R, Olive J, Wollman F-A (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim Biophys Acta 1273:150–158CrossRefGoogle Scholar
  55. Dickson VK, Silvester JA, Fearnley IM, AGW L, Walker JE (2006) On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25:2911–2918PubMedPubMedCentralCrossRefGoogle Scholar
  56. Dohnalkova AC, Kennedy DW, Mancuso J, Marshall MJ, Mainwaring PR, Fredrickson JK (2010) Characterization of pipe bomb fragments using optical microscopy and scanning electron microscopy. Microsc Microanal 16:1870–1871CrossRefGoogle Scholar
  57. Drop B, Webber-birungi M, Fusetti F, Kouril R, Kevin E, 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 286:44878–44887PubMedPubMedCentralCrossRefGoogle Scholar
  58. Drop B, Webber-Birungi M, Yadav SKN, Filipowicz-Szymanska A, Fusetti F, Boekema EJ, Croce R (2014a) Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim Biophys Acta 1837:63–72PubMedCrossRefGoogle Scholar
  59. Drop B, Yadav KNS, Boekema EJ, Croce R (2014b) Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii. Plant J 78:181–191PubMedCrossRefGoogle Scholar
  60. Dubochet J, Adrian M, Chang J-J, Homo J-C, Lepault J, McDowall AW, Schultz P (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21:129–228PubMedCrossRefGoogle Scholar
  61. Engel GS, Engel GS, Calhoun TR, Calhoun TR, Read EL, Read EL, Ahn T-K, Ahn T-K, Mancal T, Mancal T, Cheng Y-C, Cheng Y-C, Blankenship RE, Blankenship RE, Fleming GR, Fleming GR (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786PubMedCrossRefGoogle Scholar
  62. Engel BD, Schaffer M, Cuellar LK, Villa E, Plitzko JM, Baumeister W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. Elife 2015:1–29Google Scholar
  63. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  64. Finazzi G (2005) The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions. J Exp Bot 56:383–388PubMedCrossRefGoogle Scholar
  65. Fischer N, Neumann P, Konevega AL, Bock LV, Ficner R, Rodnina MV, Stark H (2015) Structure of the E. coli ribosome–EF-Tu complex at <3 Å resolution by Cs-corrected cryo-EM. Nature 520:567–570PubMedCrossRefGoogle Scholar
  66. Food and Agriculture Organisation (FAO) of the United Nations (2009) How to feed the world in 2050. 1–35Google Scholar
  67. Ford RC, Holzenburg A (2014) Organization of protein complexes and a mechanism for grana formation in photosynthetic membranes as revealed by cryo-electron microscopy. Cryst Res Technol 49:637–644CrossRefGoogle Scholar
  68. Frangakis AS, Hegerl R (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135:239–250PubMedCrossRefGoogle Scholar
  69. Fukuyama K, Hase T, Matsumoto S, Tsukihara T, Katsube Y (1980) Structure of S. platensis [2Fe-2S] ferredoxin and evolution of the chloroplast-type ferredoxins. Nature 286:522–524CrossRefGoogle Scholar
  70. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH (2002) Multicolor and electron microscopic imaging of connexin trafficking. Science 296:503–507PubMedCrossRefGoogle Scholar
  71. Gaietta GM, Giepmans BNG, Deerinck TJ, Smith WB, Ngan L, Llopis J, Adams SR, Tsien RY, Ellisman MH (2006) Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc Natl Acad Sci U S A 103:17777–17782PubMedPubMedCentralCrossRefGoogle Scholar
  72. Galaz-Montoya JG, Flanagan J, Schmid MF, Ludtke SJ (2015) Single particle tomography in EMAN2. J Struct Biol 190:279–290PubMedPubMedCentralCrossRefGoogle Scholar
  73. Garcia-Sanchez MI, Diaz-Quintana A, Gotor C, Jacquot JP, De la Rosa MA, Vega JM (2000) Homology predicted structure and functional interaction of ferredoxin from the eukaryotic alga Chlamydomonas reinhardtii with nitrite reductase and glutamate synthase. J Biol Inorg Chem 5:713–719PubMedCrossRefGoogle Scholar
  74. 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 525:121–125PubMedCrossRefGoogle Scholar
  75. Gibbons C, Montgomery MG, Leslie AG, Walker JE (2000) The structure of the central stalk in bovine F(1)-ATPase at 2.4 A resolution. Nat Struct Biol 7:1055–1061PubMedCrossRefGoogle Scholar
  76. Gold VAM, Ieva R, Walter A, Pfanner N, van der Laan M, Kühlbrandt W (2014) Visualizing active membrane protein complexes by electron cryotomography. Nat Commun 5:4129PubMedPubMedCentralCrossRefGoogle Scholar
  77. Goodenough UW, Levine RP (1969) Chloroplast ultrastructure in mutant strains of Chlamydomonas reinhardi lacking components of the photosynthetic apparatus. Plant Physiol 44:990–1000PubMedPubMedCentralCrossRefGoogle Scholar
  78. Goodenough U, Staehelin LA (1971) Structural differentiation of stacked and unstacked chloroplast membranes freeze-etch electron microscopy of wild-type and mutant strains of Chlamydomonas. J Cell Biol 48:594–619PubMedPubMedCentralCrossRefGoogle Scholar
  79. Gregory JA, Topol AB, Doerner DZ, Mayfield S (2013) Alga-produced cholera toxin-Pfs25 fusion proteins as oral vaccines. Appl Environ Microbiol 79:3917–3925PubMedPubMedCentralCrossRefGoogle Scholar
  80. Groth G, Pohl E (2001) The structure of the chloroplast F1-ATPase at 3.2 Å resolution. J Biol Chem 276:1345–1352PubMedCrossRefGoogle Scholar
  81. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342PubMedCrossRefGoogle Scholar
  82. Haehnel W, Ratajczak R, Robenek H (1989) Lateral distribution and diffusion of plastocyanin in chloroplast thylakoids. J Cell Biol 108:1397–1405PubMedCrossRefGoogle Scholar
  83. Hakulinen JK, Klyszejko AL, Hoffmann J, Eckhardt-strelau L, Brutschy B, Vonck J (2012) Structural study on the architecture of the bacterial ATP synthase F o motor. Proc Natl Acad Sci 109:2050–2056CrossRefGoogle Scholar
  84. Hasan SS, Cramer WA (2014) Internal lipid architecture of the hetero-oligomeric cytochrome b 6f complex. Structure 22:1008–1015PubMedPubMedCentralCrossRefGoogle Scholar
  85. Hasan SS, Stofleth JT, Yamashita E, Cramer WA (2013) Lipid-induced conformational changes within the cytochrome b6f complex of oxygenic photosynthesis. Biochemistry 52:2649–2654PubMedPubMedCentralCrossRefGoogle Scholar
  86. Hauer F, Gerle C, Fischer N, Oshima A, Shinzawa-Itoh K, Shimada S, Yokoyama K, Fujiyoshi Y, Stark H (2015) GraDeR: membrane protein complex preparation for single-particle cryo-EM. Structure 23:1769–1775PubMedCrossRefGoogle Scholar
  87. Heymann JB, Belnap DM (2007) Bsoft: image processing and molecular modeling for electron microscopy. J Struct Biol 157:3–18PubMedCrossRefGoogle Scholar
  88. Hippler M, Ratajczak R, Haehnel W (1989) Identification of the plastocyanin binding subunit of photosystem I. FEBS Lett 250:280–284CrossRefGoogle Scholar
  89. Hobe S, Förster R, Klingler J, Paulsen H (1995) N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34:10224–10228PubMedCrossRefGoogle Scholar
  90. Hoffmann C, Gaietta G, Zürn A, Adams SR, Terrillon S, Ellisman MH, Tsien RY, Lohse MJ (2010) Fluorescent labelling of tetracycteine-tagged proteins in intact cells. Nature 5:1666–1677Google Scholar
  91. Hrabe T, Chen Y, Pfeffer S, Kuhn Cuellar L, Mangold AV, Förster F (2012) PyTom: a python-based toolbox for localization of macromolecules in cryo-electron tomograms and subtomogram analysis. J Struct Biol 178:177–188PubMedCrossRefGoogle Scholar
  92. Huang C, Wang ZQ, Lin HN, Brumbaugh EE, Li S (1994) Interconversion of bilayer phase transition temperatures between phosphatidylethanolamines and phosphatidylcholines. Biophys Biochem Acta 1189:7–12CrossRefGoogle Scholar
  93. Huisken J, Stainier DYR (2009) Selective plane illumination microscopy techniques in developmental biology. Development 136:1963–1975PubMedPubMedCentralCrossRefGoogle Scholar
  94. Huisken J, Swoger J, Del Bene F, Wittbrodt J, Stelzer EHK (2004) Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305:1007–1009PubMedCrossRefGoogle Scholar
  95. Intergovernmental Panel on Climate Change (2014) Climate change 2014: Synthesis Report. In: Core Writing Team Pachauri RK and Meyer LA (eds) Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. IPCC, GenevaGoogle Scholar
  96. International Energy Agency (2010) World energy outlook. IEA, ParisGoogle Scholar
  97. Ito Y, Ikeguchi M (2010) Structural fluctuation and concerted motions in F1-ATPase: a molecular dynamics study. J Comput Chem 31:2175–2185PubMedCrossRefGoogle Scholar
  98. Iwai M, Takahashi Y, Minagawa J (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20:2177–2189PubMedPubMedCentralCrossRefGoogle Scholar
  99. Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213PubMedCrossRefGoogle Scholar
  100. Jans F, Mignolet E, Houyoux P-A, Cardol P, Ghysels B, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci U S A 105:20546–20551PubMedPubMedCentralCrossRefGoogle Scholar
  101. Jiang W, Hermolin J, Fillingame RH (2001) The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc Natl Acad Sci U S A 98:4966–4971PubMedPubMedCentralCrossRefGoogle Scholar
  102. Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389PubMedCrossRefGoogle Scholar
  103. Johnson UG, Porter KR (1968) Fine structure of cell division in Chlamydomonas reinhardi. Basal bodies and microtubules. J Cell Biol 38:403–425PubMedPubMedCentralCrossRefGoogle Scholar
  104. Johnson MP, Vasilev C, Olsen JD, Hunter CN (2014) Nanodomains of cytochrome b 6 f and photosystem II complexes in spinach grana thylakoid membranes. Plant Cell 26:3051–3061PubMedPubMedCentralCrossRefGoogle Scholar
  105. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917PubMedCrossRefGoogle Scholar
  106. Kabaleeswaran V, Puri N, Walker JE, Leslie AGW, Mueller DM (2006) Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase. EMBO J 25:5433–5442PubMedPubMedCentralCrossRefGoogle Scholar
  107. Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci U S A 100:98–103PubMedCrossRefGoogle Scholar
  108. Kapla J, Stevensson B, Dahlberg M, Maliniak A (2012) Molecular dynamics simulations of membranes composed of glycolipids and phospholipids. J Phys Chem B 116:244–252PubMedCrossRefGoogle Scholar
  109. 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: insights into light harvesting for PSI. J Biol Chem 278:16135–16141PubMedCrossRefGoogle Scholar
  110. Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under state 2 conditions. FEBS J 272:4797–4806PubMedCrossRefGoogle Scholar
  111. Karplus PA, Daniels MJ, Herriott JR, Herriogir JONR (1991) Atomic structure of ferredoxin-NADP+ reductase: prototype for a structurally novel flavoenzyme family. Nature 251:60–66Google Scholar
  112. Kass M, Witkin A, Terzopoulos D (1988) Snakes: active contour models. Int J Comput Vis 1:321–331CrossRefGoogle Scholar
  113. Kastner B, Fischer N, Golas MM, Sander B, Dube P, Boehringer D, Hartmuth K, Deckert J, Hauer F, Wolf E, Uchtenhagen H, Urlaub H, Herzog F, Peters JM, Poerschke D, Lührmann R, Stark H (2008) GraFix: sample preparation for single-particle electron cryomicroscopy. Nat Methods 5:53–55PubMedCrossRefGoogle Scholar
  114. Kerfeld CA, Anwar HP, Interrante R, Merchant S, Yeates TO (1995) The structure of chloroplast cytochrome c6 at 1.9 A resolution: evidence for functional oligomerization. J Mol Biol 250:627–647PubMedCrossRefGoogle Scholar
  115. Kern J, Alonso-Mori R, Tran R, Hattne J, Gildea RJ, Echols N, Gloeckner C, Hellmich J, Laksmono H, Sierra RG, Lassalle-Kaiser B, Koroidov S, Lampe A, Han G, Gul S, DiFiore D, Milathianaki D, Fry AR, Miahnahri A, Schafer DW, Messerschmidt M, Seibert MM, Koglin JE, Sokaras D, Weng T-C, Sellberg J, Latimer MJ, Grosse-Kunstleve RW, Zwart PH, White WE, Glatzel P, Adams PD, Bogan MJ, Williams GJ, Boutet S, Messinger J, Zouni A, Sauter NK, Yachandra VK, Bergmann U, Yano J (2013) Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 340:491–496PubMedPubMedCentralCrossRefGoogle Scholar
  116. Kern J, Tran R, Alonso-Mori R, Koroidov S, Echols N, Hattne J, Ibrahim M, Gul S, Laksmono H, Sierra RG, Gildea RJ, Han G, Hellmich J, Lassalle-Kaiser B, Chatterjee R, Brewster AS, Stan CA, Glockner C, Lampe A, DiFiore D, Milathianaki D, Fry AR, Seibert MM, Koglin JE, Gallo E, Uhlig J, Sokaras D, Weng TC, Zwart PH, Skinner DE, Bogan MJ, Messerschmidt M, Glatzel P, Williams GJ, Boutet S, Adams PD, Zouni A, Messinger J, Sauter NK, Bergmann U, Yano J, Yachandra VK (2014) Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. Nat Commun 5:4371PubMedPubMedCentralCrossRefGoogle Scholar
  117. Kirchhoff H, Lenhert S, Büchel C, Chi L, Nield J (2008) Probing the organization of photosystem II in photosynthetic membranes by atomic force microscopy. Biochemistry 47:431–440PubMedCrossRefGoogle Scholar
  118. Knoetzel J, Svendsen I, Simpson DJ (1992) Identification of the photosystem I antenna polypeptides in barley. Eur J Biochem 206:209–215PubMedCrossRefGoogle Scholar
  119. Kouřil R, Oostergetel GT, Boekema EJ (2011) Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochim Biophys Acta 1807:368–374PubMedCrossRefGoogle Scholar
  120. Kouril R, Strouhal O, Nosek L, Lenobel R, Chamrad I, Boekema EJ, Sebela M, Ilik P (2014) Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J 77:568–576PubMedCrossRefGoogle Scholar
  121. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580PubMedCrossRefGoogle Scholar
  122. Kudryashev M, Castaño-Díez D, Deluz C, Hassaine G, Grasso L, Graf-Meyer A, Vogel H, Stahlberg H (2016) The structure of the mouse serotonin 5-HT3 receptor in lipid vesicles. Structure 24:165–170PubMedCrossRefGoogle Scholar
  123. Kühlbrandt W (2014) The resolution revolution. Science 343:1443–1444PubMedCrossRefGoogle Scholar
  124. Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367:614–621PubMedCrossRefGoogle Scholar
  125. Kurisu G, Kusunoki M, Katoh E, Yamazaki T, Teshima K, Onda Y, Kimata-Ariga Y, Hase T (2001) Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP(+) reductase. Nat Struct Biol 8:117–121PubMedCrossRefGoogle Scholar
  126. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014PubMedCrossRefGoogle Scholar
  127. Lata S, Reichel A, Brock R, Tampé R, Piehler J (2005) High-affinity adaptors for switchable recognition of histidine-tagged proteins. J Am Chem Soc 127:10205–10215PubMedCrossRefGoogle Scholar
  128. Lemaire C, Wollman FA, Bennoun P (1988) Restoration of phototrophic growth in a mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the ATP synthase has a deletion: an example of mitochondria-dependent photosynthesis. Proc Natl Acad Sci U S A 85:1344–1348PubMedPubMedCentralCrossRefGoogle Scholar
  129. Liao M, Cao E, Julius D, Cheng Y (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107–112PubMedPubMedCentralCrossRefGoogle Scholar
  130. Lin YS, Lin JH, Chang CC (2010) Molecular dynamics simulations of the rotary motor F0 under external electric fields across the membrane. Biophys J 98:1009–1017PubMedPubMedCentralCrossRefGoogle Scholar
  131. Liss V, Barlag B, Nietschke M, Hensel M (2015) Self-labelling enzymes as universal tags for fluorescence microscopy, super-resolution microscopy and electron microscopy. Sci Rep 5:17740PubMedPubMedCentralCrossRefGoogle Scholar
  132. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428:287–292PubMedCrossRefGoogle Scholar
  133. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  134. Lučić V, Rigort A, Baumeister W (2013) Cryo-electron tomography: the challenge of doing structural biology in situ. J Cell Biol 202:407–419PubMedPubMedCentralCrossRefGoogle Scholar
  135. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, Vries AH De (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B 111: 7812–7824.Google Scholar
  136. Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR (2001) Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci U S A 98:2399–2406PubMedPubMedCentralCrossRefGoogle Scholar
  137. Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK, Sosinsky GE, Ellisman MH, Ting AY (2012) Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat Biotechnol 30:1143–1148PubMedPubMedCentralCrossRefGoogle Scholar
  138. Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 Å resolution. Elife 4:1–18CrossRefGoogle Scholar
  139. McCammon JA, Gelin BR, Karplus M (1977) Dynamics of folded proteins. Nature 267:585–590PubMedCrossRefGoogle Scholar
  140. McDonnel A, Staehelin LA (1980) Adhesion between liposomes mediated by the chlorophyll a/b light-harvesting complex isolated from chloroplast membranes. J Cell Biol 84:40–56PubMedCrossRefGoogle Scholar
  141. McDowall AW, Chang J-J, Freeman R, Lepault J, Walter A, Dubochet J (1983) Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples. J Microsc 131:1–9PubMedCrossRefGoogle Scholar
  142. Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus. Science 308:659–662PubMedCrossRefGoogle Scholar
  143. Meimberg K, Fischer N, Rochaix JD, Mühlenhoff U (1999) Lys35 of PsaC is required for the efficient photoreduction of flavodoxin by photosystem I from Chlamydomonas reinhardtii. Eur J Biochem 263:137–144PubMedCrossRefGoogle Scholar
  144. Menz RI, Walker JE, Leslie AGW (2001) Structure of bovine mitochondrial F1-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106:331–341PubMedCrossRefGoogle Scholar
  145. Meyer M, Griffiths H (2013) Origins and diversity of eukaryotic CO2-concentrating mechanisms: lessons for the future. J Exp Bot 64:769–786PubMedCrossRefGoogle Scholar
  146. Meyer Zu Tittingdorf JMW, Rexroth S, Schäfer E, Schlichting R, Giersch C, Dencher NA, Seelert H (2004) The stoichiometry of the chloroplast ATP synthase oligomer III in Chlamydomonas reinhardtii is not affected by the metabolic state. Biochim Biophys Acta 1659:92–99PubMedCrossRefGoogle Scholar
  147. Miller KR, Staehelin LA (1976) Analysis of the thylakoid outer surface. Coupling factor is limited to unstacked membrane regions. J Cell Biol 68:30–47PubMedCrossRefGoogle Scholar
  148. Minagawa J (2009) Light-harvesting proteins. In: The Chlamydomonas sourcebook, 2-vol set. Elsevier, Amsterdam, pp 503–539CrossRefGoogle Scholar
  149. Minagawa J, Han KC, Dohmae N, Takio K, Inoue Y (2001) Molecular characterization and gene expression of lhcb5 gene encoding CP26 in the light-harvesting complex II of Chlamydomonas reinhardtii. Plant Mol Biol 46:277–287PubMedCrossRefGoogle Scholar
  150. Mitome N, Suzuki T, Hayashi S, Yoshida M (2004) Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H+/ATP ratio and permissive elastic coupling. Proc Natl Acad Sci U S A 101:12159–12164PubMedPubMedCentralCrossRefGoogle Scholar
  151. Moor H, Mühlethaler K (1963) Fine structure in frozen-etched yeast cells. J Cell Biol 17:609–628PubMedPubMedCentralCrossRefGoogle Scholar
  152. Morphew MK, O’Toole ET, Page CL, Pagratis M, Meehl J, Giddings T, Gardner JM, Ackerson C, Jaspersen SL, Winey M, Hoenger A, Mcintosh JR (2015) Metallothionein as a clonable tag for protein localization by electron microscopy of cells. J Microsc 260:20–29PubMedPubMedCentralCrossRefGoogle Scholar
  153. Mullineaux CW (2014) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837:503–511PubMedCrossRefGoogle Scholar
  154. Mullineaux CW, Kirchhoff H (2007) Using fluorescence recovery after photobleaching to measure lipid diffusion in membranes. In: Dopico AM (ed) Methods in membrane lipids. Humana, Totowa, NJ, pp 267–276Google Scholar
  155. Murphy DB, Davidson MW (2012) Confocal laser scanning microscopy. In: Murphy DB, Davidson MW (eds) Fundamentals of light microscopy and electronic imaging. Wiley-Blackwell, New York, pp 265–305CrossRefGoogle Scholar
  156. Mussgnug JH, Wobbe L, Elles I, Claus C, Hamilton M, Fink A (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17:3409–3421PubMedPubMedCentralCrossRefGoogle Scholar
  157. Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5:802–814PubMedCrossRefGoogle Scholar
  158. Mustárdy L, Garab G (2003) Granum revisited. A three-dimensional model - where things fall into place. Trends Plant Sci 8:117–122PubMedCrossRefGoogle Scholar
  159. Nagayoshi M, Murase K, Fujino K, Uenishi Y, Kawamata M, Nakamura Y, Kitamura K, Higuchi I, Oku N, Hatazawa J (2005) Usefulness of noise adaptive non-linear gaussian filter in FDG-PET study. Ann Nucl Med 19:469–477PubMedCrossRefGoogle Scholar
  160. Nevo R, Charuvi D, Tsabari O, Reich Z (2012) Composition, architecture and dynamics of the photosynthetic apparatus in higher plants. Plant J 70:157–176PubMedCrossRefGoogle Scholar
  161. Nicastro D, Schwartz C, Pierson J, Gaudette R, Porter ME, McIntosh JR (2006) The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313:944–948PubMedCrossRefGoogle Scholar
  162. Nield J, Kruse O, Ruprecht J, Da Fonseca P, Büchel C, Barber J (2000) Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allows for comparison their oxygen-evolving complex organization. J Biol Chem 275:27940–27946PubMedGoogle Scholar
  163. Ogata K, Yuki T, Hatakeyama M, Uchida W, Nakamura S (2013) All-atom molecular dynamics simulation of photosystem II embedded in thylakoid membrane. J Am Chem Soc 135:15670–15673PubMedCrossRefGoogle Scholar
  164. Olive J, Vallon O (1991) Structural organization of the thylakoid membrane: freeze-fracture and immunocytochemical analysis. J Electron Microsc Tech 374:360–374CrossRefGoogle Scholar
  165. Olive J, Wollman FA, Bennoun P, Recouvreur M (1981) Ultrastructure of thylakoid membranes in C. reinhardtii: evidence for variations in the partition coefficient of the light-harvesting complex-containing particles upon membrane fracture. Arch Biochem Biophys 208:456–467PubMedCrossRefGoogle Scholar
  166. Organisation for Economic Co-Operation and Development (OECD) (2012) OECD environmental outlook to 2050. OECD, ParisGoogle Scholar
  167. Pan X, Li M, Wan T, Wang L, Jia C, Hou Z, Zhao X, Zhang J, Chang W (2011) Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat Struct Mol Biol 18:309–315PubMedCrossRefGoogle Scholar
  168. Pantelic RS, Rothnagel R, Huang C-Y, Muller D, Woolford D, Landsberg MJ, McDowall A, Pailthorpe B, Young PR, Banks J, Hankamer B, Ericksson G (2006) The discriminative bilateral filter: an enhanced denoising filter for electron microscopy data. J Struct Biol 155:395–408PubMedCrossRefGoogle Scholar
  169. Pantelic RS, Ericksson G, Hamilton N, Hankamer B (2007) Bilateral edge filter: photometrically weighted, discontinuity based edge detection. J Struct Biol 160:93–102PubMedCrossRefGoogle Scholar
  170. Pantelic RS, Meyer JC, Kaiser U, Stahlberg H (2012) The application of graphene as a sample support in transmission electron microscopy. Solid State Commun 152:1375–1382CrossRefGoogle Scholar
  171. Phuthong W, Huang Z, Wittkopp TM, Sznee K, Heinnickel ML, Dekker JP, Frese RN, Prinz FB, Grossman AR (2015) The use of contact mode atomic force microscopy in aqueous medium for structural analysis of spinach photosynthetic complexes. Plant Physiol 169:1318–1332PubMedPubMedCentralCrossRefGoogle Scholar
  172. Pogoryelov D, Yu JS, Meier T, Vonck J, Dimroth P, Muller DJ (2005) The c(15) ring of the Spirulina platensis F-ATP synthase: F-1/F-0 symmetry mismatch is not obligatory. EMBO Rep 6:1040–1044PubMedPubMedCentralCrossRefGoogle Scholar
  173. Preiner J, Horner A, Karner A, Ollinger N, Siligan C, Pohl P, Hinterdorfer P (2015) High-speed AFM images of thermal motion provide stiffness map of interfacial membrane protein moieties. Nano Lett 15:759–763PubMedCrossRefGoogle Scholar
  174. Preiss L, Klyszejko AL, Hicks DB, Liu J, Fackelmayer OJ, Yildiz Ö, Krulwich TA, Meier T (2013) The c-ring stoichiometry of ATP synthase is adapted to cell physiological requirements of alkaliphilic Bacillus pseudofirmus OF4. Proc Natl Acad Sci U S A 110:7874–7879PubMedPubMedCentralCrossRefGoogle Scholar
  175. Pribil M, Labs M, Leister D (2014) Structure and dynamics of thylakoids in land plants. J Exp Bot 65:1955–1972PubMedCrossRefGoogle Scholar
  176. Qin X, Suga M, Kuang T, Shen J-R (2015) Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348:989–995PubMedCrossRefGoogle Scholar
  177. Redinbo MR, Cascio D, Choukair MK, Rice D, Merchant S, Yeates TO (1993) The 1.5-A crystal structure of plastocyanin from the green alga Chlamydomonas reinhardtii. Biochemistry 32:10560–10567PubMedCrossRefGoogle Scholar
  178. Rees DM, Leslie AGW, Walker JE (2009) The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci U S A 106:21597–21601PubMedPubMedCentralCrossRefGoogle Scholar
  179. Renault L, Chou HT, Chiu PL, Hill RM, Zeng X, Gipson B, Zhang ZY, Cheng A, Unger V, Stahlberg H (2006) Milestones in electron crystallography. J Comput Aided Mol Des 20:519–527PubMedPubMedCentralCrossRefGoogle Scholar
  180. Ringsmuth AK, Landsberg MJ, Hankamer B (2016) Can photosynthesis enable a global transition from fossil fuels to solar fuels, to mitigate climate change and fuel-supply limitations? Renew Sustain Energy Rev 62:134–163CrossRefGoogle Scholar
  181. Ruskin RS, Yu Z, Grigorieff N (2013) Quantitative characterization of electron detectors for transmission electron microscopy. J Struct Biol 184:385–393PubMedCrossRefGoogle Scholar
  182. Russo CJ, Passmore LA (2014) Electron microscopy: ultrastable gold substrates for electron cryomicroscopy. Science 346:1377–1380PubMedPubMedCentralCrossRefGoogle Scholar
  183. Rust MJ, Bates M, Zhuang XW (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793–795PubMedPubMedCentralCrossRefGoogle Scholar
  184. Sager R, Palade GE (1954) Chloroplast structure in green and yellow strains of Chlamydomonas. Exp Cell Res 7:584–588PubMedCrossRefGoogle Scholar
  185. Sager R, Palade GE (1957) Structure and development of the chloroplast in Chlamydomonas: I. The normal green cell. J Cell Biol 3:463–488CrossRefGoogle Scholar
  186. Sakurai I, Shen JR, Leng J, Ohashi S, Kobayashi M, Wada H (2006) Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J Biochem 140:201–209PubMedCrossRefGoogle Scholar
  187. Scheller HV, Jensen PE, Haldrup A, Lunde C, Knoetzel J (2001) Role of subunits in eukaryotic photosystem I. Biochim Biophys Acta 1507:41–60PubMedCrossRefGoogle Scholar
  188. Schep DG, Zhao J, Rubinstein JL (2016) Models for the a subunits of the Thermus thermophilus V/A-ATPase and Saccharomyces cerevisiae V-ATPase enzymes by cryo-EM and evolutionary covariance. Proc Natl Acad Sci 113(12):3245–3250PubMedPubMedCentralCrossRefGoogle Scholar
  189. Schötz FA (1972) Dreidimensionale, maßstabgetreue Rekonstruktion einer grünen Flagellatenzelle nach Elektronenmikroskopie von Serienschnitten. Planta 159:152–159Google Scholar
  190. Scott KA, Bond PJ, Ivetac A, Chetwynd AP, Khalid S, Sansom MSP (2008) Coarse-grained MD simulations of membrane protein-bilayer self-assembly. Structure 16:621–630PubMedCrossRefGoogle Scholar
  191. Seelert H, Poetsch A, Dencher NA, Engel A, Stahlberg H, Müller DJ (2000) Proton-powered turbine of a plant motor. Nature 405:418–419PubMedCrossRefGoogle Scholar
  192. Sétif P (2001) Ferredoxin and flavodoxin reduction by photosystem I. Biochim Biophys Acta 1507:161–179PubMedCrossRefGoogle Scholar
  193. Sétif P, Fischer N, Lagoutte B, Bottin H, Rochaix JD (2002) The ferredoxin docking site of photosystem I. Biochim Biophys Acta 1555:204–209PubMedCrossRefGoogle Scholar
  194. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, Eastwood MP, Bank JA, Jumper JM, Salmon JK, Shan Y, Wriggers W (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330:341–346PubMedCrossRefGoogle Scholar
  195. Shimoni E, Rav-Hon O, Ohad I, Brumfeld V, Reich Z (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17:2580–2586PubMedPubMedCentralCrossRefGoogle Scholar
  196. Shroff H, Galbraith CG, Galbraith JA, White H, Gillette J, Olenych S, Davidson MW, Betzig E (2007) Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc Natl Acad Sci U S A 104:20308–20313PubMedPubMedCentralCrossRefGoogle Scholar
  197. Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM, Manley S, Sougrat R, Waterman CM, Kanchanawong P, Davidson MW, Fetter RD, Hess HF (2009) Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc Natl Acad Sci U S A 106:3125–3130PubMedPubMedCentralCrossRefGoogle Scholar
  198. Shu X, Lev-Ram V, Deerinck TJ, Qi Y, Ramko EB, Davidson MW, Jin Y, Ellisman MH, Tsien RY (2011) A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol 9Google Scholar
  199. Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76:185–196PubMedCrossRefGoogle Scholar
  200. Stahlberg H, Müller DJ, Suda K, Fotiadis D, Engel A, Meier T, Matthey U, Dimroth P (2001) Bacterial Na(+)-ATP synthase has an undecameric rotor. EMBO Rep 2:229–233PubMedPubMedCentralCrossRefGoogle Scholar
  201. Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24:919–928PubMedPubMedCentralCrossRefGoogle Scholar
  202. Stephens DJ, Allan VJ (2003) Light microscopy techniques for live cell imaging. Science 300:82–86PubMedCrossRefGoogle Scholar
  203. Stock D, Leslie AGW, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286:1700–1705PubMedCrossRefGoogle Scholar
  204. Stocker A, Keis S, Cook GM, Dimroth P (2005) Purification, crystallization, and properties of F1-ATPase complexes from the thermoalkaliphilic Bacillus sp. strain TA2.A1. J Struct Biol 152:140–145PubMedCrossRefGoogle Scholar
  205. Stoschek A, Hegerl R (1997) Denoising of electron tomographic reconstructions using multiscale transformations. J Struct Biol 120:257–265PubMedCrossRefGoogle Scholar
  206. Stroebel D, Choquet Y, Popot J-L, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418PubMedCrossRefGoogle Scholar
  207. Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen J (2014) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103PubMedCrossRefGoogle Scholar
  208. Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581PubMedPubMedCentralCrossRefGoogle Scholar
  209. Tran M, Van C, Barrera DJ, Pettersson PL, Peinado CD, Bui J, Mayfield SP (2013) Production of unique immunotoxin cancer therapeutics in algal chloroplasts. Proc Natl Acad Sci U S A 110:E15–E22PubMedCrossRefGoogle Scholar
  210. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photsystem II at a resolution of 1.9 Å. Nature 473:55–60PubMedCrossRefGoogle Scholar
  211. United Nations (2015) World population prospects: the 2015 revision, Key findings & advances tablesGoogle Scholar
  212. Vallon O, Bulte L, Dainese P, Olive J, Bassi R, Wollman FAW (1991) Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci U S A 88:8262–8266PubMedPubMedCentralCrossRefGoogle Scholar
  213. van der Heide P, Xu XP, Marsh BJ, Hanein D, Volkmann N (2007) Efficient automatic noise reduction of electron tomographic reconstructions based on iterative median filtering. J Struct Biol 158:196–204PubMedCrossRefGoogle Scholar
  214. Van Eerden FJ, De Jong DH, De Vries AH, Wassenaar TA, Marrink SJ (2015) Characterization of thylakoid lipid membranes from cyanobacteria and higher plants by molecular dynamics simulations. Biochim Biophys Acta 1848:1319–1330PubMedCrossRefGoogle Scholar
  215. Vasilev C, Brindley AA, Olsen JD, Saer RG, Beatty JT, Hunter CN (2014) Nano-mechanical mapping of the interactions between surface-bound RC-LH1-PufX core complexes and cytochrome c 2 attached to an AFM probe. Photosynth Res 120:169–180PubMedCrossRefGoogle Scholar
  216. Vassiliev S, Zaraiskaya T, Bruce D (2012) Exploring the energetics of water permeation in photosystem II by multiple steered molecular dynamics simulations. Biochim Biophys Acta 1817:1671–1678PubMedCrossRefGoogle Scholar
  217. Volkmann N (2002) A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. J Struct Biol 138:123–129PubMedCrossRefGoogle Scholar
  218. Vollmar M, Schlieper D, Winn M, Büchner C, Groth G (2009) Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J Biol Chem 284:18228–18235PubMedPubMedCentralCrossRefGoogle Scholar
  219. Vu TQ, Lam WY, Hatch EW, Lidke DS (2015) Quantum dots for quantitative imaging: from single molecules to tissue. Cell Tissue Res:71–86Google Scholar
  220. Warshel A, Levitt M (1976) Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol 103:227–249PubMedCrossRefGoogle Scholar
  221. Watanabe S, Punge A, Hollopeter G, Willig KI, Hobson RJ, Davis MW, Hell SW, Jorgensen EM (2011) Protein localization in electron micrographs using fluorescence nanoscopy. Nat Methods 8:80–84PubMedCrossRefGoogle Scholar
  222. Watt IN, Montgomery MG, Runswick MJ, Leslie AGW, Walker JE (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci U S A 107:16823–16827PubMedPubMedCentralCrossRefGoogle Scholar
  223. 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 1:1–18CrossRefGoogle Scholar
  224. White SH (2016) Membrane proteins of known 3D structure.
  225. Wollman FA, Olive J, Bennoun P, Recouvreur M (1980) Organization of the photosystem-II centers and their associated antennae in the thylakoid membranes - a comparative ultrastructural, biochemical, and biophysical study of Chlamydomonas wild-type and mutants lacking in photosystem-II reaction centers. J Cell Biol 87:728–735PubMedCrossRefGoogle Scholar
  226. Zhao C, Hellman LM, Zhan X, Bowman WS, Whiteheart SW, Fried MG (2010) Hexahistidine-tag-specific optical probes for analyses of proteins and their interactions. Anal Biochem 399:237–245PubMedCrossRefGoogle Scholar
  227. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Janina Steinbeck
    • 1
    • 2
  • Megan L. O’Mara
    • 3
  • Ian L. Ross
    • 1
  • Henning Stahlberg
    • 4
  • Ben Hankamer
    • 1
    Email author
  1. 1.Institute for Molecular BioscienceThe University of QueenslandSt LuciaAustralia
  2. 2.Westfälische Wilhelms-Universität MünsterMünsterGermany
  3. 3.Research School of ChemistryThe Australian National UniversityCanberraAustralia
  4. 4.Center for Cellular Imaging and NanoAnalytics, BiozentrumUniversity of BaselBaselSwitzerland

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