1932

Abstract

Photosynthetic membranes are typically densely packed with proteins, and this is crucial for their function in efficient trapping of light energy. Despite being crowded with protein, the membranes are fluid systems in which proteins and smaller molecules can diffuse. Fluidity is also crucial for photosynthetic function, as it is essential for biogenesis, electron transport, and protein redistribution for functional regulation. All photosynthetic membranes seem to maintain a delicate balance between crowding, order, and fluidity. How does this work in phototrophic bacteria? In this review, we focus on two types of intensively studied bacterial photosynthetic membranes: the chromatophore membranes of purple bacteria and the thylakoid membranes of cyanobacteria. Both systems are distinct from the plasma membrane, and both have a distinctive protein composition that reflects their specialized roles. Chromatophores are formed from plasma membrane invaginations, while thylakoid membranes appear to be an independent intracellular membrane system. We discuss the techniques that can be applied to study the organization and dynamics of these membrane systems, including electron microscopy techniques, atomic force microscopy, and many variants of fluorescence microscopy. We go on to discuss the insights that havebeen acquired from these techniques, and the role of membrane dynamics in the physiology of photosynthetic membranes. Membrane dynamics on multiple timescales are crucial for membrane function, from electron transport on timescales of microseconds to milliseconds to regulation and biogenesis on timescales of minutes to hours. We emphasize the open questions that remain in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-020518-120134
2020-09-08
2024-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/74/1/annurev-micro-020518-120134.html?itemId=/content/journals/10.1146/annurev-micro-020518-120134&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adams PG, Hunter CN. 2012. Adaptation of intracytoplasmic membranes to altered light intensity in Rhodobacter sphaeroides. Biochim. Biophys. Acta Bioenerg 1817:91616–27
    [Google Scholar]
  2. 2. 
    Ando T. 2018. High-speed atomic force microscopy and its future prospects. Biophys. Rev. 10:2285–92
    [Google Scholar]
  3. 3. 
    Baers LL, Breckels LM, Mills LA, Gatto L, Deery M et al. 2019. Proteome mapping of a cyanobacterium reveals distinct compartment organisation and cell-dispersed metabolism. Plant Physiol 181:1721–38
    [Google Scholar]
  4. 4. 
    Bahatyrova S, Frese RN, Siebert CA, Olsen JD, van der Werf KO et al. 2004. The native architecture of a photosynthetic membrane. Nature 430:70031058–62
    [Google Scholar]
  5. 5. 
    Béjà O, Spudich EN, Spudich JL, Leclerc M, DeLong EF 2001. Proteorhodopsin phototrophy in the ocean. Nature 411:6839786–89
    [Google Scholar]
  6. 6. 
    Binnig G, Quate CF, Gerber C 1986. Atomic force microscope. Phys. Rev. Lett. 56:9930–33
    [Google Scholar]
  7. 7. 
    Bryan SJ, Burroughs NJ, Shevela D, Yu J, Rupprecht E et al. 2014. Localisation and interactions of the Vipp1 protein in cyanobacteria. Mol. Microbiol. 94:51179–95
    [Google Scholar]
  8. 8. 
    Busselez J, Cottevieille M, Cuniasse P, Gubellini F, Boisset N, Lévy D 2007. Structural basis for the PufX-mediated dimerization of bacterial photosynthetic core complexes. Structure 15:121674–83
    [Google Scholar]
  9. 9. 
    Calzadilla PI, Zhan J, Sétif P, Lemaire C, Solymosi D et al. 2019. The cytochrome b6f complex is not involved in cyanobacterial state transitions. Plant Cell 31:4911–31
    [Google Scholar]
  10. 10. 
    Cartron ML, Olsen JD, Sener M, Jackson PJ, Brindley AA et al. 2014. Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides.Biochim.Biophys. Acta Bioenerg 1837:101769–80
    [Google Scholar]
  11. 11. 
    Casella S, Huang F, Mason D, Zhao G-Y, Johnson GN et al. 2017. Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery. Mol. Plant. 10:111434–48
    [Google Scholar]
  12. 12. 
    Chandler DE, Strümpfer J, Sener M, Scheuring S, Schulten K 2014. Light harvesting by lamellar chromatophores in Rhodospirillum photometricum. Biophys. J 106:112503–10
    [Google Scholar]
  13. 13. 
    Chidgey JW, Linhartová M, Komenda J, Jackson PJ, Dickman MJ et al. 2014. A cyanobacterial chlorophyll synthase-HliD complex associates with the Ycf39 protein and the YidC/Alb3 insertase. Plant Cell 26:31267–79
    [Google Scholar]
  14. 14. 
    Chtcheglova LA, Hinterdorfer P. 2018. Simultaneous AFM topography and recognition imaging at the plasma membrane of mammalian cells. Semin. Cell Dev. Biol. 73:45–56
    [Google Scholar]
  15. 15. 
    Cogdell RJ, Gall A, Köhler J 2006. The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q. Rev. Biophys. 39:3227–324
    [Google Scholar]
  16. 16. 
    Cooley JW, Vermaas WFJ. 2001. Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function. J. Bacteriol. 183:144251–58
    [Google Scholar]
  17. 17. 
    Drews G, Niederman RA. 2002. Membrane biogenesis in anoxygenic photosynthetic prokaryotes. Photosynth. Res. 73:187–94
    [Google Scholar]
  18. 18. 
    Engel A, Gaub HE. 2008. Structure and mechanics of membrane proteins. Annu. Rev. Biochem. 77:127–48
    [Google Scholar]
  19. 19. 
    Faulkner M, Rodriguez-Ramos J, Dykes GF, Owen SV, Casella S et al. 2017. Direct characterization of the native structure and mechanics of cyanobacterial carboxysomes. Nanoscale 9:3010662–73
    [Google Scholar]
  20. 20. 
    Faulkner M, Zhao L-S, Barrett S, Liu L-N 2019. Self-assembly stability and variability of bacterial microcompartment shell proteins in response to the environmental change. Nanoscale Res. Lett. 14:54
    [Google Scholar]
  21. 21. 
    Folea IM, Zhang P, Aro E-M, Boekema EJ 2008. Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett 582:121749–54
    [Google Scholar]
  22. 22. 
    Frain KM, Gangl D, Jones A, Zedler JAZ, Robinson C 2016. Protein translocation and thylakoid biogenesis in cyanobacteria. Biochim. Biophys. Acta Bioenerg. 1857:3266–73
    [Google Scholar]
  23. 23. 
    Frederix PLTM, Bosshart PD, Engel A 2009. Atomic force microscopy of biological membranes. Biophys. J. 96:2329–38
    [Google Scholar]
  24. 24. 
    Gao F, Zhao J, Chen L, Battchikova N, Ran Z et al. 2016. The NDH-1L-PSI supercomplex is important for efficient cyclic electron transport in cyanobacteria. Plant Physiol 172:31451–64
    [Google Scholar]
  25. 25. 
    Geyer T, Helms V. 2006. A spatial model of the chromatophore vesicles of Rhodobacter sphaeroides and the position of the cytochrome bc1 complex. Biophys. J. 91:3921–26
    [Google Scholar]
  26. 26. 
    Giliberti V, Polito R, Ritter E, Broser M, Hegemann P et al. 2019. Tip-enhanced infrared difference-nanospectroscopy of the proton pump activity of bacteriorhodopsin in single purple membrane patches. Nano Lett 19:53104–14
    [Google Scholar]
  27. 27. 
    Gonçalves RP, Bernadac A, Sturgis JN, Scheuring S 2005. Architecture of the native photosynthetic apparatus of Phaeospirillum molischianum.J. Struct. Biol 152:3221–28
    [Google Scholar]
  28. 28. 
    Heidrich J, Thurotte A, Schneider D 2017. Specific interaction of IM30/Vipp1 with cyanobacterial and chloroplast membranes results in membrane remodeling and eventually in membrane fusion. Biochim. Biophys. Acta Biomembr. 1859:4537–49
    [Google Scholar]
  29. 29. 
    Heinz S, Liauw P, Nickelsen J, Nowaczyk M 2016. Analysis of photosystem II biogenesis in cyanobacteria. Biochim. Biophys. Acta Bioenerg. 1857:3274–87
    [Google Scholar]
  30. 30. 
    Heinz S, Rast A, Shao L, Gutu A, Gügel IL et al. 2016. Thylakoid membrane architecture in Synechocystis depends on CurT, a homolog of the granal CURVATURE THYLAKOID1 proteins. Plant Cell 28:92238–60
    [Google Scholar]
  31. 31. 
    Hohmann-Marriott MF, Roberson RW. 2009. Exploring photosynthesis by electron tomography. Photosynth. Res. 102:2177–88
    [Google Scholar]
  32. 32. 
    Holmqvist O. 1979. Evidence of discontinuity between the cytoplasmic and intracytoplasmic membranes in Rhodopseudomonas sphaeroides: a study with ferrous gluconate as a tracer substance in electron microscopy and X-ray microanalysis. FEMS Microbiol. Lett. 6:137–40
    [Google Scholar]
  33. 33. 
    Hu X, Damjanović A, Ritz T, Schulten K 1998. Architecture and mechanism of the light-harvesting apparatus of purple bacteria. PNAS 95:115935–41
    [Google Scholar]
  34. 34. 
    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 464:72921210–13
    [Google Scholar]
  35. 35. 
    Johnson MP, Vasilev C, Olsen JD, Hunter CN 2014. Nanodomains of cytochrome b6f and Photosystem II complexes in spinach grana thylakoid membranes. Plant Cell 26:73051–61
    [Google Scholar]
  36. 36. 
    Joshua S, Mullineaux CW. 2004. Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:42112–19
    [Google Scholar]
  37. 37. 
    Koblízek M, Shih JD, Breitbart SI, Ratcliffe EC, Kolber ZS et al. 2005. Sequential assembly of photosynthetic units in Rhodobacter sphaeroides as revealed by fast repetition rate analysis of variable bacteriochlorophyll a fluorescence. Biochim. Biophys. Acta Bioenerg. 1706:3220–31
    [Google Scholar]
  38. 38. 
    Koepke J, Hu X, Muenke C, Schulten K, Michel H 1996. The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4:5581–97
    [Google Scholar]
  39. 39. 
    Komenda J, Sobotka R, Nixon PJ 2012. Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria. Curr. Opin. Plant Biol. 15:3245–51
    [Google Scholar]
  40. 40. 
    Konorty M, Kahana N, Linaroudis A, Minsky A, Medalia O 2008. Structural analysis of photosynthetic membranes by cryo-electron tomography of intact Rhodopseudomonas viridis cells. J. Struct. Biol. 161:3393–400
    [Google Scholar]
  41. 41. 
    Kumar S, Cartron ML, Mullin N, Qian P, Leggett GJ et al. 2017. Direct imaging of protein organization in an intact bacterial organelle using high-resolution atomic force microscopy. ACS Nano 11:1126–33
    [Google Scholar]
  42. 42. 
    Lea-Smith DJ, Bombelli P, Vasudevan R, Howe CJ 2016. Photosynthetic, respiratory and extracellular electron transport pathways in cyanobacteria. Biochim. Biophys. Acta Bioenerg. 1857:3247–55
    [Google Scholar]
  43. 43. 
    Lea-Smith DJ, Ortiz-Suarez ML, Lenn T, Nürnberg DJ, Baers LL et al. 2016. Hydrocarbons are essential for optimal cell size, division and growth of cyanobacteria. Plant Physiol 172:31928–40
    [Google Scholar]
  44. 44. 
    Liberton M, Austin JR, Berg RH, Pakrasi HB 2011. Unique thylakoid membrane architecture of a unicellular N2-fixing cyanobacterium revealed by electron tomography. Plant Physiol 155:41656–66
    [Google Scholar]
  45. 45. 
    Liberton M, Page LE, O'Dell WB, O'Neill H, Mamontov E et al. 2013. Organization and flexibility of cyanobacterial thylakoid membranes examined by neutron scattering. J. Biol. Chem. 288:53632–40
    [Google Scholar]
  46. 46. 
    Liu L-N. 2016. Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta Bioenerg. 1857:3256–65
    [Google Scholar]
  47. 47. 
    Liu L-N, Aartsma TJ, Thomas J-C, Lamers GEM, Zhou B-C, Zhang Y-Z 2008. Watching the native supramolecular architecture of photosynthetic membrane in red algae: topography of phycobilisomes and their crowding, diverse distribution patterns. J. Biol. Chem. 283:5034946–53
    [Google Scholar]
  48. 48. 
    Liu L-N, Bryan SJ, Huang F, Yu J, Nixon PJ et al. 2012. Control of electron transport routes through redox-regulated redistribution of respiratory complexes. PNAS 109:2811431–36
    [Google Scholar]
  49. 49. 
    Liu L-N, Duquesne K, Oesterhelt F, Sturgis JN, Scheuring S 2011. Forces guiding assembly of light-harvesting complex 2 in native membranes. PNAS 108:239455–59
    [Google Scholar]
  50. 50. 
    Liu L-N, Duquesne K, Sturgis JN, Scheuring S 2009. Quinone pathways in entire photosynthetic chromatophores of Rhodospirillum photometricum.J. Mol. Biol 393:127–35
    [Google Scholar]
  51. 51. 
    Liu L-N, Faulkner M, Liu X, Huang F, Darby AC, Hall N 2016. Revised genome sequence of the purple photosynthetic bacterium Blastochloris viridis. Genome Announc 4:1e01520–15
    [Google Scholar]
  52. 52. 
    Liu L-N, Scheuring S. 2013. Investigation of photosynthetic membrane structure using atomic force microscopy. Trends Plant Sci 18:5277–86
    [Google Scholar]
  53. 53. 
    Liu L-N, Sturgis JN, Scheuring S 2011. Native architecture of the photosynthetic membrane from Rhodobacter veldkampii.J. Struct. Biol 173:1138–45
    [Google Scholar]
  54. 54. 
    Llorente-Garcia I, Lenn T, Erhardt H, Harriman OL, Liu L-N et al. 2014. Single-molecule in vivo imaging of bacterial respiratory complexes indicates delocalized oxidative phosphorylation. Biochim. Biophys. Acta Bioenerg. 1837:6811–24
    [Google Scholar]
  55. 55. 
    MacGregor-Chatwin C, Jackson PJ, Sener M, Chidgey JW, Hitchcock A et al. 2019. Membrane organization of photosystem I complexes in the most abundant phototroph on Earth. Nat. Plants 5:8879–89
    [Google Scholar]
  56. 56. 
    MacGregor-Chatwin C, Sener M, Barnett SFH, Hitchcock A, Barnhart-Dailey MC et al. 2017. Lateral segregation of Photosystem I in cyanobacterial thylakoids. Plant Cell 29:51119–36
    [Google Scholar]
  57. 57. 
    McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ et al. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:6522517–21
    [Google Scholar]
  58. 58. 
    Miller LC, Zhao L-S, Canniffe DP, Martin D, Liu L-N 2020. Unfolding pathway and intermolecular interactions of the cytochrome subunit in the bacterial photosynthetic reaction center. Biochim. Biophys. Acta Bioenerg. 1861:8148204
    [Google Scholar]
  59. 59. 
    Müller DJ. 2008. AFM: A nanotool in membrane biology. Biochemistry 47:317986–98
    [Google Scholar]
  60. 60. 
    Müller DJ, Dufrêne YF. 2011. Atomic force microscopy: a nanoscopic window on the cell surface. Trends Cell Biol 21:8461–69
    [Google Scholar]
  61. 61. 
    Mullineaux CW. 2014. Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta Bioenerg. 1837:4503–11
    [Google Scholar]
  62. 62. 
    Mullineaux CW. 2014. Electron transport and light-harvesting switches in cyanobacteria. Front. Plant Sci. 5:7
    [Google Scholar]
  63. 63. 
    Mullineaux CW, Allen JF. 1990. State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II. Photosynth. Res. 23:3297–311
    [Google Scholar]
  64. 64. 
    Mullineaux CW, Tobin MJ, Jones GR 1997. Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:6658421–24
    [Google Scholar]
  65. 65. 
    Nevo R, Charuvi D, Shimoni E, Schwarz R, Kaplan A et al. 2007. Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. EMBO J 26:51467–73
    [Google Scholar]
  66. 66. 
    Niederman RA. 2016. Development and dynamics of the photosynthetic apparatus in purple phototrophic bacteria. Biochim. Biophys. Acta Bioenerg. 1857:3232–46
    [Google Scholar]
  67. 67. 
    Nielsen JT, Kulminskaya NV, Bjerring M, Linnanto JM, Rätsep M et al. 2016. In situ high-resolution structure of the baseplate antenna complex in Chlorobaculum tepidum. Nat. Commun 7:112454
    [Google Scholar]
  68. 68. 
    Niwa S, Yu L-J, Takeda K, Hirano Y, Kawakami T et al. 2014. Structure of the LH1-RC complex from Thermochromatium tepidum at 3.0 Å. Nature 508:7495228–32
    [Google Scholar]
  69. 69. 
    Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J 2010. Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 106:11–16
    [Google Scholar]
  70. 70. 
    Noble JM, Lubieniecki J, Savitzky BH, Plitzko J, Engelhardt H et al. 2018. Connectivity of centermost chromatophores in Rhodobacter sphaeroides bacteria. Mol. Microbiol. 109:6812–25
    [Google Scholar]
  71. 71. 
    Olive J, Ajlani G, Astier C, Recouvreur M, Vernotte C 1997. Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC 6803. Biochim. Biophys. Acta Bioenerg. 1319:2275–82
    [Google Scholar]
  72. 72. 
    Onoa B, Schneider AR, Brooks MD, Grob P, Nogales E et al. 2014. Atomic force microscopy of Photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids. PLOS ONE 9:7e101470
    [Google Scholar]
  73. 73. 
    Pan X, Cao D, Xie F, Xu F, Su X et al. 2020. Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nat. Commun. 11:1610
    [Google Scholar]
  74. 74. 
    Phuthong W, Huang Z, Wittkopp TM, Sznee K, Heinnickel ML et al. 2015. The use of contact mode atomic force microscopy in aqueous medium for structural analysis of spinach photosynthetic complexes. Plant Physiol 169:21318–32
    [Google Scholar]
  75. 75. 
    Pisareva T, Kwon J, Oh J, Kim S, Ge C et al. 2011. Model for membrane organization and protein sorting in the cyanobacterium Synechocystis sp. PCC 6803 inferred from proteomics and multivariate sequence analyses. J. Proteome Res. 10:83617–31
    [Google Scholar]
  76. 76. 
    Pullerits T, Sundström V. 1996. Photosynthetic light-harvesting pigment−protein complexes: toward understanding how and why. Acc. Chem. Res. 29:8381–89
    [Google Scholar]
  77. 77. 
    Qian P, Bullough PA, Hunter CN 2008. Three-dimensional reconstruction of a membrane-bending complex: the RC-LH1-PufX core dimer of Rhodobacter sphaeroides. J. Biol. Chem 283:2014002–11
    [Google Scholar]
  78. 78. 
    Qian P, Siebert CA, Wang P, Canniffe DP, Hunter CN 2018. Cryo-EM structure of the Blastochloris viridis LH1-RC complex at 2.9 Å. Nature 556:7700203–8
    [Google Scholar]
  79. 79. 
    Rast A, Schaffer M, Albert S, Wan W, Pfeffer S et al. 2019. Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane. Nat. Plants 5:4436–46
    [Google Scholar]
  80. 80. 
    Rengstl B, Oster U, Stengel A, Nickelsen J 2011. An intermediate membrane subfraction in cyanobacteria is involved in an assembly network for Photosystem II biogenesis. J. Biol. Chem. 286:2421944–51
    [Google Scholar]
  81. 81. 
    Rexroth S, Mullineaux CW, Ellinger D, Sendtko E, Rogner M, Koenig F 2011. The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23:62379–90
    [Google Scholar]
  82. 82. 
    Ritz T, Park S, Schulten K 2001. Kinetics of excitation migration and trapping in the photosynthetic unit of purple bacteria. J. Phys. Chem. B 105:348259–67
    [Google Scholar]
  83. 83. 
    Roszak AW, Howard TD, Southall J, Gardiner AT, Law CJ et al. 2003. Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 302:56521969–72
    [Google Scholar]
  84. 84. 
    Sacharz J, Bryan SJ, Yu J, Burroughs NJ, Spence EM et al. 2016. Sub-cellular location of FtsH proteases in the cyanobacterium Synechocystis sp. PCC 6803 suggests localised PSII repair zones in the thylakoid membranes. Mol. Microbiol. 96:3448–62
    [Google Scholar]
  85. 85. 
    Saer RG, Blankenship RE. 2017. Light harvesting in phototrophic bacteria: structure and function. Biochem. J. 474:132107–31
    [Google Scholar]
  86. 86. 
    Sarcina M, Bouzovitis N, Mullineaux CW 2006. Mobilization of photosystem II induced by intense red light in the cyanobacterium Synechococcus sp PCC7942. Plant Cell 18:2457–64
    [Google Scholar]
  87. 87. 
    Sarcina M, Mullineaux CW. 2004. Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J. Biol. Chem. 279:3536514–18
    [Google Scholar]
  88. 88. 
    Sarcina M, Murata N, Tobin MJ, Mullineaux CW 2003. Lipid diffusion in the thylakoid membranes of the cyanobacterium Synechococcus sp.: effect of fatty acid desaturation. FEBS Lett 553:3295–98
    [Google Scholar]
  89. 89. 
    Sarcina M, Tobin MJ, Mullineaux CW 2001. Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942: effects of phycobilisome size, temperature, and membrane lipid composition. J. Biol. Chem. 276:5046830–34
    [Google Scholar]
  90. 90. 
    Schägger H, Pfeiffer K. 2000. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19:81777–83
    [Google Scholar]
  91. 91. 
    Scheuring S, Busselez J, Lévy D 2005. Structure of the dimeric PufX-containing core complex of Rhodobacter blasticus by in situ atomic force microscopy. J. Biol. Chem. 280:21426–31
    [Google Scholar]
  92. 92. 
    Scheuring S, Nevo R, Liu L-N, Mangenot S, Charuvi D et al. 2014. The architecture of Rhodobacter sphaeroides chromatophores. Biochim. Biophys. Acta Bioenerg. 1837:81263–70
    [Google Scholar]
  93. 93. 
    Scheuring S, Rigaud J-L, Sturgis JN 2004. Variable LH2 stoichiometry and core clustering in native membranes of Rhodospirillum photometricum. EMBO J 23:214127–33
    [Google Scholar]
  94. 94. 
    Scheuring S, Seguin J, Marco S, Lévy D, Robert B, Rigaud J-L 2003. Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. PNAS 100:41690–93
    [Google Scholar]
  95. 95. 
    Scheuring S, Sturgis JN. 2005. Chromatic adaptation of photosynthetic membranes. Science 309:5733484–87
    [Google Scholar]
  96. 96. 
    Scheuring S, Sturgis JN. 2009. Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery. Photosynth. Res. 102:2197–211
    [Google Scholar]
  97. 97. 
    Selão TT, Zhang L, Knoppová J, Komenda J, Norling B 2015. Photosystem II assembly steps take place in the thylakoid membrane of the cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol 57:195–104
    [Google Scholar]
  98. 98. 
    Şener MK, Olsen JD, Hunter CN, Schulten K 2007. Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle. PNAS 104:4015723–28
    [Google Scholar]
  99. 99. 
    Shashkova S, Leake MC. 2017. Single-molecule fluorescence microscopy review: shedding new light on old problems. Biosci. Rep. 37:4BSR20170031
    [Google Scholar]
  100. 100. 
    Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW et al. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15:92152–64
    [Google Scholar]
  101. 101. 
    Singharoy A, Maffeo C, Delgado-Magnero KH, Swainsbury DJK, Sener M et al. 2019. Atoms to phenotypes: molecular design principles of cellular energy metabolism. Cell 179:51098–111
    [Google Scholar]
  102. 102. 
    Stengel A, Gügel IL, Hilger D, Rengstl B, Jung H, Nickelsen J 2012. Initial steps of Photosystem II de novo assembly and preloading with manganese take place in biogenesis centers in Synechocystis. Plant Cell 24:2660–75
    [Google Scholar]
  103. 103. 
    Stingaciu L-R, O'Neill HM, Liberton M, Pakrasi HB, Urban VS 2019. Influence of chemically disrupted photosynthesis on cyanobacterial thylakoid dynamics in Synechocystis sp. PCC 6803. Sci. Rep. 9:15711
    [Google Scholar]
  104. 104. 
    Stingaciu L-R, O'Neill H, Liberton M, Urban VS, Pakrasi HB, Ohl M 2016. Revealing the dynamics of thylakoid membranes in living cyanobacterial cells. Sci. Rep. 6:119627
    [Google Scholar]
  105. 105. 
    Sun Y, Wollman AJM, Huang F, Leake MC, Liu L-N 2019. Single-organelle quantification reveals stoichiometric and structural variability of carboxysomes dependent on the environment. Plant Cell 31:71648–64
    [Google Scholar]
  106. 106. 
    Sundström V, Pullerits T, van Grondelle R 1999. Photosynthetic light-harvesting: Reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J. Phys. Chem. B 103:132327–46
    [Google Scholar]
  107. 107. 
    Sutter M, Faulkner M, Aussignargues C, Paasch BC, Barrett S et al. 2016. Visualization of bacterial microcompartment facet assembly using high-speed atomic force microscopy. Nano Lett 16:31590–95
    [Google Scholar]
  108. 108. 
    Tucker JD, Siebert CA, Escalante M, Adams PG, Olsen JD et al. 2010. Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles. Mol. Microbiol. 76:4833–47
    [Google Scholar]
  109. 109. 
    Uchihashi T, Scheuring S. 2018. Applications of high-speed atomic force microscopy to real-time visualization of dynamic biomolecular processes. Biochim. Biophys. Acta Gen. Subj. 1862:2229–40
    [Google Scholar]
  110. 110. 
    van de Meene AML, Hohmann-Marriott MF, Vermaas WFJ, Roberson RW 2006. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol. 184:5259–70
    [Google Scholar]
  111. 111. 
    Vermaas WFJ, Timlin JA, Jones HDT, Sinclair MB, Nieman LT et al. 2008. In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells. PNAS 105:104050–55
    [Google Scholar]
  112. 112. 
    Verméglio A, Lavergne J, Rappaport F 2016. Connectivity of the intracytoplasmic membrane of Rhodobacter sphaeroides: a functional approach. Photosynth. Res. 127:113–24
    [Google Scholar]
  113. 113. 
    Wada H, Murata N. 1998. Membrane lipids in cyanobacteria. Lipids in Photosynthesis: Structure, Function and Genetics P-A Siegenthaler, N Murata 65–81 Dordrecht, Neth.: Springer
    [Google Scholar]
  114. 114. 
    Westphal S, Heins L, Soll J, Vothknecht UC 2001. Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis. PNAS 98:74243–48
    [Google Scholar]
  115. 115. 
    Wood WHJ, MacGregor-Chatwin C, Barnett SFH, Mayneord GE, Huang X et al. 2018. Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer. Nat. Plants 4:2116–27
    [Google Scholar]
  116. 116. 
    Xin Y, Shi Y, Niu T, Wang Q, Niu W et al. 2018. Cryo-EM structure of the RC-LH core complex from an early branching photosynthetic prokaryote. Nat. Commun. 9:11568
    [Google Scholar]
  117. 117. 
    Yu L-J, Suga M, Wang-Otomo Z-Y, Shen J-R 2018. Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution. Nature 556:7700209–13
    [Google Scholar]
  118. 118. 
    Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB 2001. The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. PNAS 98:2313443–48
    [Google Scholar]
  119. 119. 
    Zhao L-S, Huokko T, Wilson S, Simpson DM, Wang Q et al. 2020. Structural variability, coordination, and adaptation of a native photosynthetic machinery. Nat. Plants 6:869–82
    [Google Scholar]
  120. 120. 
    Zhao L-S, Su H-N, Li K, Xie B-B, Liu L-N et al. 2016. Supramolecular architecture of photosynthetic membrane in red algae in response to nitrogen starvation. Biochim. Biophys. Acta Bioenerg. 1857:111751–58
    [Google Scholar]
/content/journals/10.1146/annurev-micro-020518-120134
Loading
/content/journals/10.1146/annurev-micro-020518-120134
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error