Dissecting the Native Architecture and Dynamics of Cyanobacterial Photosynthetic Machinery

Molecular Plant

Volumn 10, Issue 11, 2017, Pages 1434-1448

  Casella, Selene ^a   Huang, Fang ^a   Mason, David ^a   Zhao, Guo Yan ^a,b   Johnson, Giles N ^c   Mullineaux, Conrad W ^d   Liu, Lu Ning ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b SHANDONG NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

atomic force microscopy; cyanobacteria; fluorescence imaging; photosynthesis; protein dynamics; thylakoid membrane

Indexed keywords

ATOMIC FORCE MICROSCOPY; CYANOBACTERIUM; GENETICS; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PHYSIOLOGY; THYLAKOID;

CYANOBACTERIA; MICROSCOPY, ATOMIC FORCE; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; THYLAKOIDS;

EID: 85033401291     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2017.09.019     Document Type: Article

References (80)

1. Acin-Perez, R., Fernandez-Silva, P., Peleato, M.L., Perez-Martos, A., Enriquez, J.A., Respiratory active mitochondrial supercomplexes. Mol. Cell 32 (2008), 529–539.
2. Agarwal, R., Matros, A., Melzer, M., Mock, H.P., Sainis, J.K., Heterogeneity in thylakoid membrane proteome of Synechocystis 6803. J. Proteomics 73 (2010), 976–991.
3. Ardail, D., Privat, J.P., Egret-Charlier, M., Levrat, C., Lerme, F., Louisot, P., Mitochondrial contact sites. Lipid composition and dynamics. J. Biol. Chem. 265 (1990), 18797–18802.
4. Bečková, M., Gardian, Z., Yu, J., Konik, P., Nixon, P.J., Komenda, J., Association of Psb28 and Psb27 proteins with PSII-PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to high light. Mol. Plant 10 (2017), 62–72.
5. Checchetto, V., Segalla, A., Allorent, G., La Rocca, N., Leanza, L., Giacometti, G.M., Uozumi, N., Finazzi, G., Bergantino, E., Szabo, I., Thylakoid potassium channel is required for efficient photosynthesis in cyanobacteria. Proc. Natl. Acad. Sci. USA 109 (2012), 11043–11048.
6. Collins, A.M., Liberton, M., Jones, H.D., Garcia, O.F., Pakrasi, H.B., Timlin, J.A., Photosynthetic pigment localization and thylakoid membrane morphology are altered in Synechocystis 6803 phycobilisome mutants. Plant Physiol. 158 (2012), 1600–1609.
7. Consoli, E., Croce, R., Dunlap, D.D., Finzi, L., Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep. 6 (2005), 782–786.
8. DeRuyter, Y.S., Fromme, P., Molecular structure of the photosynthetic apparatus. Herrero, A., Flores, E., (eds.) The Cyanobacteria: Molecular Biology, Genomics, and Evolution, 2008, Caister Academic Press, Norfolk, UK, 217–270.
9. Dupuy, A.D., Engelman, D.M., Protein area occupancy at the center of the red blood cell membrane. Proc. Natl. Acad. Sci. USA 105 (2008), 2848–2852.
10. El-Mohsnawy, E., Kopczak, M.J., Schlodder, E., Nowaczyk, M., Meyer, H.E., Warscheid, B., Karapetyan, N.V., Rogner, M., Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry 49 (2010), 4740–4751.
11. Engel, B.D., Schaffer, M., Kuhn Cuellar, L., Villa, E., Plitzko, J.M., Baumeister, W., Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. Elife, 4, 2015, e04889.
12. Fechner, P., Boudier, T., Mangenot, S., Jaroslawski, S., Sturgis, J.N., Scheuring, S., Structural information, resolution, and noise in high-resolution atomic force microscopy topographs. Biophys. J. 96 (2009), 3822–3831.
13. Folea, I.M., Zhang, P., Aro, E.M., Boekema, E.J., Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett. 582 (2008), 1749–1754.
14. Fraser, J.M., Tulk, S.E., Jeans, J.A., Campbell, D.A., Bibby, T.S., Cockshutt, A.M., Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942. PLoS One, 8, 2013, e59861.
15. Frick, M., Schmidt, K., Nichols, B.J., Modulation of lateral diffusion in the plasma membrane by protein density. Curr. Biol. 17 (2007), 462–467.
16. 6/f complex. Plant Cell Physiol. 28 (1987), 1547–1553.
17. Gao, F., Zhao, J., Chen, L., Battchikova, N., Ran, Z., Aro, E.M., Ogawa, T., Ma, W., The NDH-1L-PSI supercomplex is important for efficient cyclic electron transport in cyanobacteria. Plant Physiol. 172 (2016), 1451–1464.
18. Golden, S.S., Mutagenesis of cyanobacteria by classical and gene-transfer-based methods. Methods Enzymol. 167 (1988), 714–727.
19. 0-ATP synthase and ADP/ATP translocator. Testing a hypothesis for ATP synthesis in the mitochondrial inner membrane. Biochim. Biophys. Acta 1069 (1991), 131–138.
20. Gust, B., Chandra, G., Jakimowicz, D., Yuqing, T., Bruton, C.J., Chater, K.F., Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv. Appl. Microbiol. 54 (2004), 107–128.
21. Gust, B., Kieser, T., Chater, K.F., REDIRECT Technology: PCR-Targeting System in Streptomyces coelicolor. 2002, John Innes Centre, Norwich.
22. Hochman, J.H., Schindler, M., Lee, J.G., Ferguson-Miller, S., Lateral mobility of cytochrome c on intact mitochondrial membranes as determined by fluorescence redistribution after photobleaching. Proc. Natl. Acad. Sci. USA 79 (1982), 6866–6870.
23. Iwai, M., Takizawa, K., Tokutsu, R., Okamuro, A., Takahashi, Y., Minagawa, J., Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464 (2010), 1210–1213.
24. Iwai, M., Yokono, M., Nakano, A., Toward understanding the multiple spatiotemporal dynamics of chlorophyll fluorescence. Plant Signal. Behav., 10, 2015, e1022014.
25. Johnson, A.S., van Horck, S., Lewis, P.J., Dynamic localization of membrane proteins in Bacillus subtilis. Microbiology 150 (2004), 2815–2824.
26. 6f and photosystem II complexes in spinach grana thylakoid membranes. Plant Cell 26 (2014), 3051–3061.
27. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., Krauss, N., Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411 (2001), 909–917.
28. Joshua, S., Bailey, S., Mann, N.H., Mullineaux, C.W., Involvement of phycobilisome diffusion in energy quenching in cyanobacteria. Plant Physiol. 138 (2005), 1577–1585.
29. Joshua, S., Mullineaux, C.W., Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol. 135 (2004), 2112–2119.
30. Joshua, S., Mullineaux, C.W., The rpaC gene product regulates phycobilisome-photosystem II interaction in cyanobacteria. Biochim. Biophys. Acta 1709 (2005), 58–68.
31. Kirchhoff, H., Molecular crowding and order in photosynthetic membranes. Trends Plant Sci. 13 (2008), 201–207.
32. Kirchhoff, H., Haferkamp, S., Allen, J.F., Epstein, D.B., Mullineaux, C.W., Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol. 146 (2008), 1571–1578.
33. Kirchhoff, H., Mukherjee, U., Galla, H.J., Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41 (2002), 4872–4882.
34. Kirchhoff, H., Tremmel, I., Haase, W., Kubitscheck, U., Supramolecular photosystem II organization in grana thylakoid membranes: evidence for a structured arrangement. Biochemistry 43 (2004), 9204–9213.
35. Kruip, J., Boekema, E.J., Bald, D., Boonstra, A.F., Rogner, M., Isolation and structural characterization of monomeric and trimeric photosystem I complexes (P700.FA/FB and P700.FX) from the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 268 (1993), 23353–23360.
36. Kruip, J., Bald, D., Boekema, E., Rogner, M., Evidence for the existence of trimeric and monomeric Photosystem I complexes in thylakoid membranes from cyanobacteria. Photosynth. Res. 40 (1994), 279–286.
37. Kruip, J., Chitnis, P.R., Lagoutte, B., Rögner, M., Boekema, E.J., Structural organization of the major subunits in cyanobacterial photosystem 1. Localization of subunits PsaC, -D, -E, -F, and -J. J. Biol. Chem. 272 (1997), 17061–17069.
38. + channels: from crystal structures to diversity. FEMS Microbiol. Rev. 29 (2005), 961–985.
39. Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970), 680–685.
40. Lapuente-Brun, E., Moreno-Loshuertos, R., Acin-Perez, R., Latorre-Pellicer, A., Colas, C., Balsa, E., Perales-Clemente, E., Quiros, P.M., Calvo, E., Rodriguez-Hernandez, M.A., et al. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340 (2013), 1567–1570.
41. Lea-Smith, D.J., Ross, N., Zori, M., Bendall, D.S., Dennis, J.S., Scott, S.A., Smith, A.G., Howe, C.J., Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol. 162 (2013), 484–495.
42. Lenn, T., Leake, M.C., Mullineaux, C.W., Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo. Mol. Microbiol. 70 (2008), 1397–1407.
43. Liu, L.N., Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta 1857 (2016), 256–265.
44. Liu, L.N., Scheuring, S., Investigation of photosynthetic membrane structure using atomic force microscopy. Trends Plant Sci. 18 (2013), 277–286.
45. Liu, L.N., Aartsma, T.J., Thomas, J.C., Zhou, B.C., Zhang, Y.Z., FRAP analysis on red alga reveals the fluorescence recovery is ascribed to intrinsic photoprocesses of phycobilisomes than large-scale diffusion. PLoS One, 4, 2009, e5295.
46. Liu, L.N., Duquesne, K., Sturgis, J.N., Scheuring, S., Quinone pathways in entire photosynthetic chromatophores of Rhodospirillum photometricum. J. Mol. Biol. 393 (2009), 27–35.
47. Liu, L.N., Sturgis, J.N., Scheuring, S., Native architecture of the photosynthetic membrane from Rhodobacter veldkampii. J. Struct. Biol. 173 (2011), 138–145.
48. Liu, L.N., Bryan, S.J., Huang, F., Yu, J.F., Nixon, P.J., Rich, P.R., Mullineaux, C.W., Control of electron transport routes through redox-regulated redistribution of respiratory complexes. Proc. Natl. Acad. Sci. USA 109 (2012), 11431–11436.
49. Liu, H., Zhang, H., Niedzwiedzki, D.M., Prado, M., He, G., Gross, M.L., Blankenship, R.E., Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342 (2013), 1104–1107.
50. Llorente-Garcia, I., Lenn, T., Erhardt, H., Harriman, O.L., Liu, L.N., Robson, A., Chiu, S.W., Matthews, S., Willis, N.J., Bray, C.D., et al. Single-molecule in vivo imaging of bacterial respiratory complexes indicates delocalized oxidative phosphorylation. Biochim. Biophys. Acta 1837 (2014), 811–824.
51. MacGregor-Chatwin, C., Sener, M., Barnett, S.F., Hitchcock, A., Barnhart-Dailey, M.C., Maghlaoui, K., Barber, J., Timlin, J.A., Schulten, K., Hunter, C.N., Lateral segregation of photosystem I in cyanobacterial thylakoids. Plant Cell 29 (2017), 1119–1136.
52. McConnell, M.D., Koop, R., Vasil'ev, S., Bruce, D., Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol. 130 (2002), 1201–1212.
53. Mörschel, E., Schatz, G.H., Correlation of photosystem-II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172 (1987), 145–154.
54. Mullineaux, C.W., FRAP analysis of photosynthetic membranes. J. Exp. Bot. 55 (2004), 1207–1211.
55. Mullineaux, C.W., Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim. Biophys. Acta 1837 (2014), 503–511.
56. Mullineaux, C.W., Emlyn-Jones, D., State transitions: an example of acclimation to low-light stress. J. Exp. Bot. 56 (2005), 389–393.
57. Mullineaux, C.W., Sarcina, M., Probing the dynamics of photosynthetic membranes with fluorescence recovery after photobleaching. Trends Plant Sci. 7 (2002), 237–240.
58. Mullineaux, C.W., Tobin, M.J., Jones, G.R., Mobility of photosynthetic complexes in thylakoid membranes. Nature 390 (1997), 421–424.
59. Murphy, D.J., The molecular organisation of the photosynthetic membranes of higher plants. Biochim. Biophys. Acta 864 (1986), 33–94.
60. Nehls, S., Snapp, E.L., Cole, N.B., Zaal, K.J., Kenworthy, A.K., Roberts, T.H., Ellenberg, J., Presley, J.F., Siggia, E., Lippincott-Schwartz, J., Dynamics and retention of misfolded proteins in native ER membranes. Nat. Cell Biol. 2 (2000), 288–295.
61. Phuthong, W., Huang, Z., Wittkopp, T.M., Sznee, K., Heinnickel, M.L., Dekker, J.P., Frese, R.N., Prinz, F.B., Grossman, A.R., The use of contact mode atomic force microscopy in aqueous medium for structural analysis of spinach photosynthetic complexes. Plant Physiol. 169 (2015), 1318–1332.
62. Rexroth, S., Mullineaux, C.W., Ellinger, D., Sendtko, E., Rogner, M., Koenig, F., The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23 (2011), 2379–2390.
63. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., Stanier, R.Y., Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111 (1979), 1–61.
64. Sarcina, M., Mullineaux, C.W., Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J. Biol. Chem. 279 (2004), 36514–36518.
65. Sarcina, M., Tobin, M.J., Mullineaux, C.W., 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 (2001), 46830–46834.
66. Sarcina, M., Murata, N., Tobin, M.J., Mullineaux, C.W., Lipid diffusion in the thylakoid membranes of the cyanobacterium Synechococcus sp.: effect of fatty acid desaturation. FEBS Lett. 553 (2003), 295–298.
67. Sarcina, M., Bouzovitis, N., Mullineaux, C.W., Mobilization of photosystem II induced by intense red light in the cyanobacterium Synechococcus sp PCC7942. Plant Cell 18 (2006), 457–464.
68. Scheuring, S., Boudier, T., Sturgis, J.N., From high-resolution AFM topographs to atomic models of supramolecular assemblies. J. Struct. Biol. 159 (2007), 268–276.
69. Sherman, D.M., Troyan, T.A., Sherman, L.A., Localization of membrane proteins in the cyanobacterium Synechococcus sp. PCC7942 (Radial asymmetry in the photosynthetic complexes). Plant Physiol. 106 (1994), 251–262.
70. Stingaciu, L.R., O'Neill, H., Liberton, M., Urban, V.S., Pakrasi, H.B., Ohl, M., Revealing the dynamics of thylakoid membranes in living cyanobacterial cells. Sci. Rep., 6, 2016, 19627.
71. Tremmel, I.G., Kirchhoff, H., Weis, E., Farquhar, G.D., Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim. Biophys. Acta 1607 (2003), 97–109.
72. Turconi, S., Schweitzer, G., Holzwarth, A.R., Temperature dependence of picosecond fluorescence kinetics of a cyanobacterial photosystem I particle. Photochem. Photobiol. 57 (1993), 113–119.
73. Umena, Y., Kawakami, K., Shen, J.R., Kamiya, N., Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473 (2011), 55–60.
74. Vermaas, W.F., Photosynthesis and Respiration in Cyanobacteria. In: Encyclopedia of Life Sciences. 2001, Nature Publishing Group, London, 245–251.
75. Vermaas, W.F., Timlin, J.A., Jones, H.D., Sinclair, M.B., Nieman, L.T., Hamad, S.W., Melgaard, D.K., Haaland, D.M., In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells. Proc. Natl. Acad. Sci. USA 105 (2008), 4050–4055.
76. Vogel, F., Bornhovd, C., Neupert, W., Reichert, A.S., Dynamic subcompartmentalization of the mitochondrial inner membrane. J. Cell Biol. 175 (2006), 237–247.
77. Watanabe, M., Semchonok, D.A., Webber-Birungi, M.T., Ehira, S., Kondo, K., Narikawa, R., Ohmori, M., Boekema, E.J., Ikeuchi, M., Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc. Natl. Acad. Sci. USA 111 (2014), 2512–2517.
78. Wilkens, V., Kohl, W., Busch, K., Restricted diffusion of OXPHOS complexes in dynamic mitochondria delays their exchange between cristae and engenders a transitory mosaic distribution. J. Cell Sci. 126 (2013), 103–116.
79. Zanetti, M., Teardo, E., La Rocca, N., Zulkifli, L., Checchetto, V., Shijuku, T., Sato, Y., Giacometti, G.M., Uozumi, N., Bergantino, E., et al. A novel potassium channel in photosynthetic cyanobacteria. PLoS One, 5, 2010, e10118.
80. Zhang, P., Battchikova, N., Jansen, T., Appel, J., Ogawa, T., Aro, E.M., Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803. Plant Cell 16 (2004), 3326–3340.