Summary
The primary reactions of purple bacterial photosynthesis take place in two pigment-protein complexes, the peripheral LH2 complex and the core RC-LH1 complex. In order to understand any type of excitation-energy transfer in the LH system detailed knowledge about the correlation between the geometrical structure and the nature of the electronically excited states is crucial. The interplay between the geometrical arrangement of the pigments and the transition probabilities of the various exciton states leads to key spectral features, such as narrow lines, that are clearly visible with single-molecule spectroscopy but are averaged out in conventional ensemble experiments. Combining low-temperature single-molecule spectroscopy with numerical simulations has allowed us to achieve a refined structural model for the bacteriochlorophyll a (BChl a) pigment arrangement in RC-LH1 core complexes of Rps. palustris. The experimental data are consistent with an equidistant arrangement of 15 BChl a dimers on an ellipse, where each dimer has been taken homologeous to those from the B850 pigment pool of LH2 from Rps. acidophila.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
R.J. Cogdell, A. Gall, J. Köhler, The architecture and function of purple bacteria: from single molecules to in vivo membranes. Quart. Rev. Biophys. 39, 227–324 (2006)
X. Hu, T. Ritz, A. Damjanovic, F. Autenrieth, K. Schulten, Photosynthetic apparatus of purple bacteria. Quart. Rev. Biophys. 35, 1–62 (2002)
G. McDermott, S.M. Prince, A.A. Freer, A.M. Hawthornthwaite-Lawless, M.Z. Papiz, R.J. Cogdell, N.W. Isaacs, Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374, 517–521 (1995)
J. Koepke, X. Hu, C. Muenke, K. Schulten, H. Michel, The crystal structure of the light harvesting complex II (B800–B850) from Rhodospirillum molischianum. Structure 4, 581–597 (1996)
K. McLuskey, S.M. Prince, R.J. Cogdell, N.W. Isaacs, The crystallographic structure of the B800–820 Lh3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila Strain 7050. Biochem. 40, 8783–8789 (2001)
M.Z. Papiz, S.M. Prince, T. Howard, R.J. Cogdell, N.W. Isaacs, The structure and thermal motion of the B800–850 LH2 complex from Rps. acidophila at 2.0 (A)over-circle resolution and 100 K: new structural features and functionally relevant motions. J. Mol. Biol. 326, 1523–1538 (2003)
T.J. Aartsma, J. Matysik, Advanced in Photosynthesis and Respiration. Vol. 26: Biophysical Techniques in Photosynthesis, Vol. II (Springer, Dordrecht, 2008)
B. Grimm, R.J. Porra, R. Wolfhart, H. Scheer, in Advances in Photosynthesis and Respiration Vol. 25: Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications (Series ed. Govindjee) (Springer, Dordrecht, 2004)
A. Aird, J. Wrachtrup, K. Schulten, C. Tietz, Possible pathway for ubiquinone shuttling in Rhodospirillum rubrum revealed by molecular dynamics simulation. Biophys. J. 92, 23–33 (2007)
U. Gerken, D. Lupo, C. Tietz, J. Wrachtrup, R. Ghosh, Circular symmetry of the light-harvesting 1 complex from Rhodospirillum rubrum is not perturbed by interaction with the reaction center. Biochemistry 42, 10354–10360 (2003)
H. Stahlberg, J. Dubochet, H. Vogel, R. Gosh, Are the light harvesting I complexes from Rhodospirillum rubrum arranged around the reaction centre in a square geometry? J. Mol. Biol. 282, 819–831 (1998)
S. Scheuring, F. Francia, J. Busselez, B.A. Melandri, J.L. Rigaud, D. Levy, Structural role of Pufx in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides. J. Biol. Chem. 279, 3620–3626 (2004)
C.A. Siebert, P. Qian, D. Fotiadis, A. Engel, C.N. Hunter, P.A. Bullough, Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the Role of Pufx. EMBO J. 23, 690–700 (2004)
R.P. Goncalves, J. Busselez, D. Levy, J. Seguin, S. Scheuring, Membrane insertion of Rhodopseudomonas acidophila light harvesting complex 2 investigated by high resolution AFM. J. Struct. Biol. 149, 79–86 (2005)
D. Fotiadis, P. Qian, A. Philippsen, P.A. Bullough, A. Engel, C.N. Hunter, 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 (2004)
S. Bahatyrova, R.N. Frese, C.A. Siebert, J.D. Olsen, K.O. van der Werf, R. van Grondelle, R.A. Niederman, P.A. Bullough, C. Otto, C.N. Hunter, The native architecture of a photosynthetic membrane. Nature 430, 1058–1062 (2004)
S. Karrasch, P.A. Bullough, R. Ghosh, The 8.5 Å projection map of the light harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J. 14, 631–638 (1995)
F. Francia, J. Wang, G. Venturoli, B.A. Melandri, W.P. Barz, D. Oesterhelt, The reaction center-LH1 antenna complex of Rhodobacter sphaeroides contains one pufx molecule which is involved in dimerization of this complex. Biochemistry 38, 6834–6845 (1999)
A.W. Roszak, T.D. Howard, J. Southall, A.T. Gardiner, C.J. Law, N.W. Isaacs, R. Cogdell, Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 302, 1969–1971 (2003)
P. Qian, C. Neil Hunter, P.A. Bullough, The 8.5 A projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides. J. Mol. Biol. 349, 948–960 (2005)
S. Scheuring, R.P. Goncalves, V. Prima, J.N. Sturgis, The photosynthetic apparatus of Rhodopseudomonas palustris: structures and organization. J. Mol. Biol. 358, 83–96 (2006)
T. Pullerits, V. Sundström, Photosynthetic light-harvesting pigment-protein complexes: toward understanding how and why. Acc. Chem. Res. 29, 381–389 (1996)
H.-M. Wu, M. Rätsep, I.-J. Lee, R.J. Cogdell, G.J. Small, Exciton level structure and energy disorder of the B850 ring of the LH2 antenna complex. J. Phys. Chem. B 101, 7654–7663 (1997a)
T.M.H. Creemers, C. de Caro, R.W. Visschers, R. van Grondelle, S. Völker, Spectral hole burning and fluorescence line narrowing in subunits of the light harvesting complex LH1 of purple bacteria. J. Phys. Chem. B 103, 9770–9776 (1999)
V. Sundström, T. Pullerits, R. van Grondelle, Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J. Phys. Chem. B 103, 2327–2346 (1999)
M.A. Bopp, Y. Jia, L. Li, R.J. Cogdell, R.M. Hochstrasser, Fluorescence and photobleaching dynamics of single light-harvesting complexes. Proc. Natl. Acad. Sci. 94, 10630–10635 (1997)
M.A. Bopp, A. Sytnik, T.D. Howard, R.J. Cogdell, R.M. Hochstrasser, The dynamics of structural deformations of immobilized single light-harvesting complexes. Proc. Natl. Acad. Sci. 96, 11271–11276 (1999)
D. Rutkauskas, R. Novoderezkhin, R.J. Cogdell, R. van Grondelle, Fluorescence spectral fluctuations of single LH2 complexes from Rhodopseudomonas acidophila strain 10050. Biochemistry 43, 4431–4438 (2004)
D. Rutkauskas, V. Novoderezhkin, R.J. Cogdell, R. van Grondelle, Fluorescence spectroscopy of conformational changes of single LH2 complexes. Biophys. J. 88, 422–435 (2005)
V.I. Novoderezhkin, D. Rutkauskas, R. Van Grondelle, Multistate conformational model of a single LH2 complex: quantitative picture of time-dependent spectral fluctuations. Chem. Phys. 341, 45–56 (2007)
C. Tietz, O. Cheklov, A. Draebenstedt, J. Schuster, J. Wrachtrup, Spectroscopy on single light-harvesting complexes at low temperature. J. Phys. Chem. B 103, 6328–6333 (1999)
A.M. van Oijen, M. Ketelaars, J. Köhler, T.J. Aartsma, J. Schmidt, Unraveling the electronic structure of individual photosynthetic pigment-protein complexes. Science 285, 400–402 (1999)
M. Ketelaars, C. Hofmann, J. Köhler, T.D. Howard, R.J. Cogdell, J. Schmidt, T.J. Aartsma, Spectroscopy on individual light-harvesting 1 complexes of Rhodopseudomonas acidophila. Biophys. J. 83, 1701–1715 (2002)
C. Hofmann, T.J. Aartsma, J. Köhler, Energetic disorder and the B850-exciton states of individual light-harvesting 2 complexes from Rhodopseudomonas acidophila. Chem. Phys. Lett. 395, 373–378 (2004a)
M. Ketelaars, J.M. Segura, S. Oellerich, W.P.F. de Ruijter, G. Magis, T.J. Aartsma, M. Matsushita, J. Schmidt, R.J. Cogdell, J. Köhler, Probing the electronic structure and conformational flexibility of individual light-harvesting 3 complexes by optical single-molecule spectroscopy. J. Phys. Chem. B 110, 18710–18717 (2006)
W.P.F. de Ruijter, J.M. Segura, R.J. Cogdell, A.T. Gardiner, S. Oellerich, T.J. Aartsma, Fluorescence-emission spectroscopy of individual LH2 and LH3 complexes: Ultrafast Dynamics of Molecules in the Condensed Phase: Photon Echoes and Coupled Excitations - A Tribute to Douwe A. Wiersma. Chem. Phys. 341, 320–325 (2007)
M.F. Richter, J. Baier, R.J. Cogdell, J. Köhler, S. Oellerich, Single-molecule spectroscopic characterization of light-harvesting 2 complexes reconstituted into model membranes. Biophys. J. 93, 183–191 (2007a)
M. Ketelaars, A.M. van Oijen, M. Matsushita, J. Köhler, J. Schmidt, T.J. Aartsma, Spectroscopy on the B850 band of individual light-harvesting 2 complexes of Rhodopseudomonas acidophila: I. Experiments and Monte-Carlo simulations. Biophys. J. 80, 1591–1603 (2001)
M.V. Mostovoy, J. Knoester, Statistics of optical spectra from single ring aggregates and its application to LH2. J. Phys. Chem. B 104, 12355–12364 (2000)
S. Jang, S.E. Dempster, R.J. Silbey, Characterization of the static disorder in the B850 band of LH2. J. Phys. Chem. B 105, 6655–6665 (2001)
M. Matsushita, M. Ketelaars, A.M. van Oijen, J. Köhler, T.J. Aartsma, J. Schmidt, Spectroscopy on the B850 band of individual light-harvesting 2 complexes of Rhodopseudomonas acidophila: II. Exciton states of an elliptically deformed ring aggregate. Biophys. J. 80, 1604–1614 (2001)
C. Hofmann, F. Francia, G. Venturoli, D. Oesterhelt, J. Köhler, Energy transfer in a single self-aggregated photosynthetic unit. FEBS Lett. 546, 345–348 (2003a)
C. Hofmann, M. Ketelaars, M. Matsushita, H. Michel, T.J. Aartsma, J. Köhler, Single-molecule study of the electronic couplings in a circular array of molecules: Light-harvesting-2 complex from Rhodospirillum molischianum. Phys. Rev. Lett. 90, 013004 (2003b)
C. Hofmann, H. Michel, M. van Heel, J. Köhler, Multivariate analysis of single-molecule spectra: Surpassing spectral diffusion. Phys. Rev. Lett. 94, 195501 (2005)
C. Hofmann, T.J. Aartsma, H. Michel, J. Köhler, Direct observation of tiers in the energy landscape of a chromoprotein: A single-molecule study. Proc. Natl. Acad. Sci. 100, 15534–15538 (2003c)
C. Hofmann, T.J. Aartsma, H. Michel, J. Köhler, Spectral dynamics in the B800 band of LH2 from Rhodospirillum molischianum: A single-molecule study. New J. Phys. 6, 1–15 (2004b)
J. Baier, M.F. Richter, R.J. Cogdell, S. Oellerich,, J. Köhler, Do proteins at low temperature behave as glasses? A single-molecule study. J. Phys. Chem. B 111, 1135–1138 (2007)
J. Baier, M.F. Richter, R.J. Cogdell, S. Oellerich, J. Köhler, Determination of the spectral diffusion kernel of a protein by single molecule spectroscopy. Phys. Rev. Lett. 100, 8108–1–4 (2008)
H. Oikawa, S. Fujiyoshi, T. Dewa, M. Nango, M. Matsushita, How deep is the potential well confining a protein in a specific conformation? A single-molecule study on temperature dependence of conformational change between 5 and 18 K. J. Am. Chem. Soc. 130, 4580–4581 (2008)
T. Aartsma, J. Köhler, Optical spectroscopy of individual light-harvesting complexes, in Advanced in Photosynthesis and Respiration. Vol. 26: Biophysical Techniques in Photosynthesis, Vol. II, ed. by T.J. Aartsma, J. Matysik (Springer, Dordrecht, 2008), pp. 241–266
J. Köhler, T.J. Aartsma, Single molecule spectroscopy of pigment protein complexes from purple bacteria, in Advances in Photosynthesis and Respiration Vol. 25: Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications (Series ed. Govindjee), ed. by B. Grimm, R.J. Porra, R. Wolfhart, H. Scheer (Springer, Dordrecht, 2004), pp. 309–321
Y. Berlin, A. Burin, J. Friedrich, J. Köhler, Low temperature spectroscopy of proteins. Part II: Experiments with single protein complexes. Phys. Life Rev. 4, 64–89 (2007)
A.S. Davidov, Theory of Molecular Excitons (Plenum, New York, 1971)
M.F. Richter, J. Baier, T. Prem, S. Oellerich, F. Francia, G. Venturoli, D. Oesterhelt, J. Southall, R.J. Cogdell, J. Köhler, Symmetry matters for the electronic structure of core complexes from Rhodopseudomonas palustris and Rhodobacter sphaeroides PufX. Proc. Natl. Acad. Sci. 104, 6661–6665 (2007c)
J. Knoester, V.M. Agranovich, Frenkel and charge-transfer excitions in organic solids, in Thin Films and Nanostructures Vol. 31, ed. by V.M. Agranovich, C.F. Bassani (Elsevier, San Diego, CA, 2003), pp. 1–96
H.-M. Wu, N.R.S. Reddy, G.J. Small, Direct observation and hole burning of the lowest exciton level (B870) of the LH2 antenna complex of Rhodopseudomonas acidophila (strain 10050). J. Phys. Chem. B 101, 651–656 (1997b)
H.-M. Wu, M. Rätsep, R. Jankowiak, R.J. Cogdell, G.J. Small, Hole burning and absorption studies of the LH1 antenna complex of purple bacteria: Effects of pressure and temperature. J. Phys. Chem. B 102, 4023–4034 (1998)
K. Timpmann, Z. Katiliene, N.W. Woodbury, A. Freiberg, Exciton self trapping in one-dimensional photosynthetic antennas. J. Phys. Chem. B 105, 12223–12225 (2001)
K. Timpmann, M. Rätsep, C.N. Hunter, A. Freiberg, Emitting excitonic polaron states in Core LH1 and peripheral LH2 bacterial light-harvesting complexes. J. Phys. Chem. B 108, 10581–10588 (2004)
M. Richter, J. Baier, J. Southall, R. Cogdell, S. Oellerich, J. Köhler, Spectral diffusion of the lowest exciton component in the core complex from Rhodopseudomonas palustris studied by single-molecule spectroscopy. Photosynth. Res. 95, 285–290 (2008)
M. Richter, J. Baier, J. Southall, R. Cogdell, S. Oellerich, J. Köhler, Spectral diffusion of the lowest exciton component in the core complex from Rhodopseudomonas palustris studied by single-molecule spectroscopy. Photosynth. Res. 95, 285–290 (2008)
M.F. Richter, J. Baier, J. Southall, R.J. Cogdell, S. Oellerich, J. Köhler, Refinement of the x-ray structure of the RC LH1 core complex from Rhodopseudomonas palustris by single-molecule spectroscopy. Proc. Natl. Acad. Sci. 104, 20280–20284 (2007b)
Acknowledgements
We thank June Southall for the preparation of the light-harvesting complexes. RJC thanks the BBSRC for funding.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Richter, M.F., Baier, J., Cogdell, R.J., Oellerich, S., Köhler, J. (2010). The Influence of Symmetry on the Electronic Structure of the Photosynthetic Pigment-Protein Complexes from Purple Bacteria. In: Gräslund, A., Rigler, R., Widengren, J. (eds) Single Molecule Spectroscopy in Chemistry, Physics and Biology. Springer Series in Chemical Physics, vol 96. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02597-6_26
Download citation
DOI: https://doi.org/10.1007/978-3-642-02597-6_26
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-02596-9
Online ISBN: 978-3-642-02597-6
eBook Packages: Physics and AstronomyPhysics and Astronomy (R0)