Abstract
Photosynthesis both in the past and present provides the vast majority of the energy used on the planet. The purple photosynthetic bacteria are a group of organisms that are able to perform photosynthesis using a particularly simple system that has been much studied. The main molecular constituents required for photosynthesis in these organisms are a small number of transmembrane pigment–protein complexes. These are able to function together with a high quantum efficiency (about 95%) to convert light energy into chemical potential energy. While the structure of the various proteins have been solved for several years, direct studies of the supramolecular assembly of these complexes in native membranes needed maturity of the atomic force microscope (AFM). Here, we review the novel findings and the direct conclusions that could be drawn from high-resolution AFM analysis of photosynthetic membranes. These conclusions rely on the possibility that the AFM brings of obtaining molecular resolution images of large membrane areas and thereby bridging the resolution gap between atomic structures and cellular ultrastructure.
Similar content being viewed by others
References
Allen JP, Feher G, Yeates TO, Komiya H et al (1987a) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84(16):5730–5734
Allen JP, Feher G, Yeates TO, Komiya H et al (1987b) Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84(17):6162–6166
Ando T, Kodera N, Takai E, Maruyama D et al (2001) A high-speed atomic force microscope for studying biological macromolecules. Proc Natl Acad Sci USA 98:12468–12472
Bahatyrova S, Frese RN, Siebert CA, Olsen JD et al (2004a) The native architecture of a photosynthetic membrane. Nature 430(7003):1058–1062
Bahatyrova S, Frese RN, van der Werf KO, Otto C et al (2004b) Flexibility and size heterogeneity of the lh1 light harvesting complex revealed by atomic force microscopy: functional significance for bacterial photosynthesis. J Biol Chem 279(20):21327–21333
Baksh MM, Jaros M, Groves JT (2004) Detection of molecular interactions at membrane surfaces through colloid phase transitions. Nature 427(6970):139–141
Berry EA, Huang LS, Saechao LK, Pon NG et al (2004) X-ray structure of Rhodobacter capsulatus cytochrome bc (1): comparison with its mitochondrial and chloroplast counterparts. Photosynth Res 81(3):251–275
Binning G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56:930–933
Binning G, Gerber C, Stoll E, Albrecht TR et al (1987) Atomic resolution with atomic force microscopy. Europhys Lett 3:1281–1286
Bowyer JR, Hunter CN, Ohnishi T, Niederman RA (1985) Photosynthetic membrane development in Rhodopseudomonas sphaeroides. Spectral and kinetic characterization of redox components of light-driven electron flow in apparent photosynthetic membrane growth initiation sites. J Biol Chem 260(6):3295–3304
Broglie RM, Hunter CN, Delepelaire P, Niederman RA et al (1980) Isolation and characterization of the pigment-protein complexes of Rhodopseudomonas sphaeroides by lithium dodecyl sulfate/polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 77(1):87–91
Butt HJ (1992) Measuring local surface charge densities in electrolyte solutions with a scanning force microscope. Biophys J 63:578–582
Buzhynskyy N, Girmens JF, Faigle W, Scheuring S (2007a) Human cataract lens membrane at subnanometer resolution. J Mol Biol 374(1):162–169
Buzhynskyy N, Hite RK, Walz T, Scheuring S (2007b) The supramolecular architecture of junctional microdomains in native lens membranes. EMBO Rep 8(1):51–5
Cheung CL, Hafner JH, Lieber CM (2000) Carbon nanotube atomic force microscopy tips: direct growth by chemical vapor deposition and application to high-resolution imaging. Proc Natl Acad Sci USA 97:3809–3813
Cohen-Bazire G, Kunisawa R (1963) The fine structure of Rhodospirillum rubrum. J Cell Biol 16:401–419
Comayras F, Jungas C, Lavergne J (2005) Functional consequences of the organization of the photosynthetic apparatus in Rhodobacter sphaeroides. I. Quinone domains and excitation transfer in chromatophores and reaction center.antenna complexes. J Biol Chem 280(12):11203–11213
Deisenhofer J, Michel H (1989) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. Biosci Rep 9(4):383–419
Deisenhofer J, Epp O, Miki K, Huber R et al (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180(2):385–398
Deisenhofer J, Epp O, Sinning I, Michel H (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 246(3):429–457
Destainville N (2008) Cluster phases of membrane proteins. Phys Rev E Stat Nonlin Soft Matter Phys 77(1 Pt 1):011905
Drews G (1960) Studies on the substructure of “chromatophores” of Rhodospirillum rubrum and Rhodospirillum molischianum. Arch Mikrobiol 36:99–108
Drews G, Giesbreacht P (1963) On the morphogenesis of bacterial “chromatophores” (thylakoids) and on the synthesis of bacteriochlorophyll in Rhodopseudomonas spheroides and Rhodospirillum rubrum. Zentralbl Bakteriol 190:508–535
Engel A (2003) Robert feulgen lecture. microscopic assessment of membrane protein structure and function. Histochem Cell Biol 120:93–102
Esser L, Gong X, Yang S, Yu L et al (2006) Surface-modulated motion switch: capture and release of iron-sulfur protein in the cytochrome bc1 complex. Proc Natl Acad Sci USA 103(35):13045–13050
Esser L, Elberry M, Zhou F, Yu CA et al (2008) Inhibitor-complexed structures of the cytochrome bc1 from the photosynthetic bacterium Rhodobacter sphaeroides. J Biol Chem 283(5):2846–2857
Evans M, Hawthornthwaite AM, Cogdell RJ (1990) Isolation and characterisation of the different b800–850 light-harvesting complexes from low- and high-light grown cells of Rhodopseudomonas palustris, strain. Biochim Biophys Acta 1016:71–76
Fassioli F, Olaya-Castro A, Scheuring S, Sturgis JN et al (2009) Energy transfer in light-adapted photosynthetic membranes: from active to saturated photosynthesis. Proc Natl Acad Sci USA. submitted
Fechner P, Boudier T, Mangenot S, Jaroslawski S et al (2009) Structural information, resolution and noise in high-resolution atomic force microscopy topographs. Biophys J
Fotiadis D, Qian P, Philippsen A, Bullough PA et al (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy. J Biol Chem 279:2063–2068
Freer A, Prince S, Sauer K, Papiz M et al (1996) Pigment-pigment interactions and energy transfer in the antenna complex of the photosynthetic bacterium Rhodopseudomonas acidophila. Structure 4(4):449–462
Frese RN, Pàmies JC, Olsen JD, Bahatyrova S et al (2008) Protein shape and crowding drive domain formation and curvature in biological membranes. Biophys J 94(2):640–647
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(3):921–926
Glaser EG, Meinhardt SW, Crofts AR (1984) Reduction of cytochrome b-561 through the antimycin-sensitive site of the ubiquinol-cytochrome c2 oxidoreductase complex of Rhodopseudomonas sphaeroides. FEBS Lett 178(2):336–342
Goldsbury C, Scheuring S (2002) Introduction to atomic force microscopy (afm) in biology. Curr Protoc Protein Sci Chapter 17:Unit 17.7
Goldsbury C, Kistler J, Aebi U, Arvinte T et al (1999) Watching amyloid fibrils grow by time-lapse atomic force microscopy. J Mol Biol 285(1):33–39
Gonçalves RP, Bernadac A, Sturgis JN, Scheuring S (2005) Architecture of the native photosynthetic apparatus of Phaeospirillum molischianum. J Struct Biol 152(3):221–228
Hansma HG, Hoh JH (1994) Biomolecular imaging with the atomic force microscope. Annu Rev Biophys Biomol Struct 23:115–139
Heberle J, Riesle J, Thiedemann G, Oesterhelt D et al (1994) Proton migration along the membrane surface and retarded surface to bulk transfer. Nature 370(6488):379–382
Hess S, Akesson E, Cogdell RJ, Pullerits T et al (1995) Energy transfer in spectrally inhomogeneous light-harvesting pigment-protein complexes of purple bacteria. Biophys J 69(6):2211–2225
Hu X, Schulten K (1998) Model for the light-harvesting complex I (B875) of Rhodobacter sphaeroides. Biophys J 75(2):683–694
Hu X, Ritz T, Damjanović A, Autenrieth F et al (2002) Photosynthetic apparatus of purple bacteria. Q Rev Biophys 35(1):1–62
Hunter CN, Pennoyer JD, Sturgis JN, Farrelly D et al (1988) Oligomerization states and associations of light-harvesting pigment-protein complexes of Rhodobacter sphaeroides as analyzed by lithium dodecyl sulfate polyacrylamide gel electrophoresis. Biochemistry 27:3459–3467
Israelachvili J (1991) Intermolecular & surface forces. Academic Press, London
Israelachvili J, Wennerstom H (1996) Role of hydration and water structure in biological and colloidal interactions. Nature 379:219–225
Jaschke PR, Leblanc HN, Lang AS, Beatty JT (2008) The pucc protein of rhodobacter capsulatus mitigates an inhibitory effect of light-harvesting 2 alpha and beta proteins on light-harvesting complex 1. Photosynth Res 95(2-3):279–284
Karrasch S, Bullough PA, Ghosh R (1995) The 8.5 a projection map of the light-harvesting complex i from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J 14(4):631–638
Koepke J, Hu X, Muenke C, Schulten K et al (1996) The crystal structure of the light-harvesting complex ii (b800-850) from rhodospirillum molischianum. Structure 4(5):581–597
Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302(5647):1009–1014
Lancaster CR, Bibikova MV, Sabatino P, Oesterhelt D et al (2000) Structural basis of the drastically increased initial electron transfer rate in the reaction center from a Rhodopseudomonas viridis mutant described at 2.00 Å resolution. J Biol Chem 275(50):39364–39368
Lavergne J, Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Biochem Sci 16(4):129–134
Mascle-Allemand C, Lavergne J, Bernadac A, Sturgis JN (2008) Organisation and function of Phaeospirillum molischianum photosynthetic apparatus. Biochim Biophys Acta 1777(12):1552–1559
Mascle-Allemand C, Duquesne K, Lebrun R, Scheuring S et al (2009) Antenna mixing in photosynthetic membranes from Phaeospirillum molischianum (submitted)
McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, et al (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521
Monger TG, Parson WW (1977) Singlet-triplet fusion in Rhodopseudomonas sphaeroides chromatophores. A probe of the organization of the photosynthetic apparatus. Biochim Biophys Acta 460(3):393–407
Möller C, Allen M, Elings V, Engel A, Müller DJ (1999) Tapping mode atomic force microscopy produces faithful high-resolution images of protein surfaces. Biophys J 77:1050–1058
Müller DJ, Amrein M, Engel A (1997) Adsorption of biological molecules to a solid support for scanning probe microscopy. J Struct Biol 119(2):172–188
Müller DJ, Baumeister W, Engel A (1999a) Controlled unzipping of a bacterial surface layer with atomic force microscopy. Proc Natl Acad Sci USA 96(23):13170–13174
Müller DJ, Fotiadis D, Scheuring S, Müller SA et al (1999b) Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscope. Biophys J 76(2):1101–1111
Müller DJ, Heymann JB, Oesterhelt F, Möller C et al (2000) Atomic force microscopy of native purple membrane. Biochim Biophys Acta 1460(1):27–38
Müller DJ, Sapra KT, Scheuring S, Kedrov A et al (2006) Single-molecule studies of membrane proteins. Curr Opin Struct Biol 16(4):489–495
Oelze J, Drews G (1972) Membranes of photosynthetic bacteria. Biochim Biophys Acta 265(2):209–239
Qian P, Hunter CN, Bullough PA (2005) The 8.5 Å projection structure of the core rc-lh1-pufx dimer of Rhodobacter sphaeroides. J Mol Biol 349(5):948–960
Roszak AW, Howard TD, Southall J, Gardiner AT et al (2003) Crystal structure of the rc-lh1 core complex from Rhodopseudomonas palustris. Science 302(5652):1969–1972
Schabert FA, Engel A (1994) Reproducible acquisition of Escherichia coli porin surface topographs by atomic force microscopy. Biophys J 67(6):2394–2403
Schabert FA, Henn C, Engel A (1995) Native Escherichia coli ompf porin surfaces probed by atomic force microscopy. Science 268(5207):92–94
Scheuring S (2006) AFM studies of the supramolecular assembly of bacterial photosynthetic core-complexes. Curr Opin Chem Biol 10(5):387–393
Scheuring S, Sturgis JN (2005) Chromatic adaptation of photosynthetic membranes. Science 309(5733):484–487
Scheuring S, Sturgis JN (2006) Dynamics and diffusion in photosynthetic membranes from Rhodospirillum photometricum. Biophys J 91(10):3707–3717
Scheuring S, Reiss-Husson F, Engel A, Rigaud JL et al (2001) High resolution topographs of the Rubrivivax gelatinosus light-harvesting complex 2. EMBO J 20:3029–3035
Scheuring S, Seguin J, Marco S, Lévy D et al (2003a) AFM characterization of tilt and intrinsic flexibility of rhodobacter sphaeroides light harvesting complex 2 (LH2). J Mol Biol 325(3):569–580
Scheuring S, Seguin J, Marco S, Lévy D et al (2003b) Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. atomic force microscopy. Proc Natl Acad Sci USA 100(4):1690–1693
Scheuring S, Francia F, Busselez J, Melandri BA et al (2004a) Structural role of pufx in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides. J Biol Chem 279(5):3620–3626
Scheuring S, Rigaud JL, Sturgis JN (2004b) Variable LH2 stoichiometry and core clustering in native membranes of Rhodospirillum photometricum. EMBO J 23(21):4127–4133
Scheuring S, Sturgis JN, Prima V, Bernadac A et al (2004c) Watching the photosynthetic apparatus in native membranes. Proc Natl Acad Sci USA 101(31):11293–11297
Scheuring S, Busselez J, Lévy D (2005a) Structure of the dimeric pufx-containing core complex of Rhodobacter blasticus by in situ atomic force microscopy. J Biol Chem 280(2):1426–1431
Scheuring S, Lévy D, Rigaud JL (2005b) Watching the components of photosynthetic bacterial membranes and their in situ organisation by atomic force microscopy. Biochim Biophys Acta 1712(2):109–127
Scheuring S, Gonçalves RP, Prima V, Sturgis JN (2006) The photosynthetic apparatus of Rhodopseudomonas palustris: structures and organization. J Mol Biol 358(1):83–96
Scheuring S, Boudier T, Sturgis JN (2007) From high-resolution AFM topographs to atomic models of supramolecular assemblies. J Struct Biol 159(2):268–76
Seelert H, Poetsch A, Dencher NA, Engel A et al (2000) Structural biology. Proton-powered turbine of a plant motor. Nature 405(6785):418–419
Sener MK, Schulten K (2008) From atomic-level structure to supramolecular organization in the photosynthetic unit of purple bacteria. In: Hunter CN, Daldal F, Thurnauer MC, Beatty TJ (eds) The purple phototrophic bacteria. Vol. 28 of Advances in photosynthesis and respiration. Springer, New York, pp 275–294
Sener MK, Olsen JD, Hunter CN, Schulten K (2007) Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle. Proc Natl Acad Sci USA 104(40):15723–15728
Siebert CA, Qian P, Fotiadis D, Engel A et al (2004) Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of pufx. EMBO J 23:690–700
Stamouli A, Kafi S, Klein DCG, Oosterkamp TH et al (2003) The ring structure and organization of light harvesting 2 complexes in a reconstituted lipid bilayer, resolved by atomic force microscopy. Biophys J 84(4):2483–2491
Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426(6965):413–418
Sturgis JN, Niedermann RA (1996) The effect of different levels of the B800-850 light-harvesting complex on intracytoplasmic membrane development in Rhodobacter sphaeroides. Arch Microbiol 165(4):235–242
Sturgis JN, Niederman RA (2008) Atomic force microscopy reveals multiple patterns of antenna organization in purple bacteria: implications for energy transduction mechanisms and membrane modeling. Photosynth Res 95(2-3):269–278
Verméglio A, Joliot P (1999) The photosynthetic apparatus of Rhodobacter sphaeroides. Trends Microbiol 7(11):435–440
Viani MB, Pietrasanta LI, Thompson JB, Chand A et al (2000) Probing protein-protein interactions in real time. Nat Struct Biol 7(8):644–647
Walz T, Ghosh R (1997) Two-dimensional crystallization of the light-harvesting I-reaction centre photounit from Rhodospirillum rubrum. J Mol Biol 265(2):107–111
Xia D, Yu CA, Kim H, Xia JZ et al (1997) Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science 277(5322):60–66
Xia D, Esser L, Elberry M, Zhou F et al (2008) The road to the crystal structure of the cytochrome bc (1) complex from the anoxigenic, photosynthetic bacterium Rhodobacter sphaeroides. J Bioenerg Biomembr 40(5):485–492
Yeates TO, Komiya H, Rees DC, Allen JP et al (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: membrane-protein interactions. Proc Natl Acad Sci USA 84(18):6438–6442
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Scheuring, S., Sturgis, J.N. Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery. Photosynth Res 102, 197–211 (2009). https://doi.org/10.1007/s11120-009-9413-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-009-9413-7