Skip to main content

Advertisement

Log in

Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bahatyrova S, Frese RN, Siebert CA, Olsen JD et al (2004a) The native architecture of a photosynthetic membrane. Nature 430(7003):1058–1062

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Baksh MM, Jaros M, Groves JT (2004) Detection of molecular interactions at membrane surfaces through colloid phase transitions. Nature 427(6970):139–141

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Binning G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56:930–933

    Article  Google Scholar 

  • Binning G, Gerber C, Stoll E, Albrecht TR et al (1987) Atomic resolution with atomic force microscopy. Europhys Lett 3:1281–1286

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Butt HJ (1992) Measuring local surface charge densities in electrolyte solutions with a scanning force microscope. Biophys J 63:578–582

    Article  PubMed  CAS  Google Scholar 

  • Buzhynskyy N, Girmens JF, Faigle W, Scheuring S (2007a) Human cataract lens membrane at subnanometer resolution. J Mol Biol 374(1):162–169

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cohen-Bazire G, Kunisawa R (1963) The fine structure of Rhodospirillum rubrum. J Cell Biol 16:401–419

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Deisenhofer J, Michel H (1989) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. Biosci Rep 9(4):383–419

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Destainville N (2008) Cluster phases of membrane proteins. Phys Rev E Stat Nonlin Soft Matter Phys 77(1 Pt 1):011905

    PubMed  Google Scholar 

  • Drews G (1960) Studies on the substructure of “chromatophores” of Rhodospirillum rubrum and Rhodospirillum molischianum. Arch Mikrobiol 36:99–108

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Engel A (2003) Robert feulgen lecture. microscopic assessment of membrane protein structure and function. Histochem Cell Biol 120:93–102

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hansma HG, Hoh JH (1994) Biomolecular imaging with the atomic force microscope. Annu Rev Biophys Biomol Struct 23:115–139

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Schulten K (1998) Model for the light-harvesting complex I (B875) of Rhodobacter sphaeroides. Biophys J 75(2):683–694

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Ritz T, Damjanović A, Autenrieth F et al (2002) Photosynthetic apparatus of purple bacteria. Q Rev Biophys 35(1):1–62

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Israelachvili J (1991) Intermolecular & surface forces. Academic Press, London

    Google Scholar 

  • Israelachvili J, Wennerstom H (1996) Role of hydration and water structure in biological and colloidal interactions. Nature 379:219–225

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lavergne J, Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Biochem Sci 16(4):129–134

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Oelze J, Drews G (1972) Membranes of photosynthetic bacteria. Biochim Biophys Acta 265(2):209–239

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schabert FA, Engel A (1994) Reproducible acquisition of Escherichia coli porin surface topographs by atomic force microscopy. Biophys J 67(6):2394–2403

    Article  PubMed  CAS  Google Scholar 

  • Schabert FA, Henn C, Engel A (1995) Native Escherichia coli ompf porin surfaces probed by atomic force microscopy. Science 268(5207):92–94

    Article  PubMed  CAS  Google Scholar 

  • Scheuring S (2006) AFM studies of the supramolecular assembly of bacterial photosynthetic core-complexes. Curr Opin Chem Biol 10(5):387–393

    Article  PubMed  CAS  Google Scholar 

  • Scheuring S, Sturgis JN (2005) Chromatic adaptation of photosynthetic membranes. Science 309(5733):484–487

    Article  PubMed  CAS  Google Scholar 

  • Scheuring S, Sturgis JN (2006) Dynamics and diffusion in photosynthetic membranes from Rhodospirillum photometricum. Biophys J 91(10):3707–3717

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426(6965):413–418

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Verméglio A, Joliot P (1999) The photosynthetic apparatus of Rhodobacter sphaeroides. Trends Microbiol 7(11):435–440

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simon Scheuring.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-009-9413-7

Keywords

Navigation