International Journal of Bioorganic Chemistry

| Peer-Reviewed |

Interactions of Photosynthetic Reaction Centers with Bc1 Complexes from Rhodobacter Sphaeroides Studied Using SEIRAS on a Nano-Structured Gold Surface

Received: 29 January 2017    Accepted: 21 February 2017    Published: 22 March 2017
Views:       Downloads:

Share This Article

Abstract

Inter-protein reactions of photosynthetic reaction centers (RCs) with bc1 complexes from R. sphaeroides, have been investigated using surface-enhanced Infrared-absorption spectroscopy (SEIRAS). Surface enhancement was achieved by a nano-structured gold surface. The proteins were immobilized via his-tags attached to the P side of the RC and the C-terminal end of the cytochrome (cyt) b subunit and co-reconstituted into a lipid bilayer by in-situ dialysis. In this configuration, the cyt c binding site of the two proteins is located on opposite sides of the membrane. Light-minus-dark absorbance spectra under continuous illumination in the absence of an electron donor indicated a slow quinone/semiquinone exchange, allowing release of ubiquinol (QH2) into the membrane. The interaction of the bc1 with QH2 was indicated by the stationary state obtained but only in the presence of cyt c. The interaction is discussed in terms of a semiquinone species formed in the course of the Q cycle mechanism of the bc1.

DOI 10.11648/j.ijbc.20170202.13
Published in International Journal of Bioorganic Chemistry (Volume 2, Issue 2, June 2017)
Page(s) 61-69
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Photosynthetic Reaction Centers, Bc1 Complexes, R. Sphaeroides, Surface-Enhanced Infrared-Absorption Spectroscopy, Nano-Structured Gold Surface, Ubiquinol, Semiquinone, His-Tags

References
[1] Giess, F, Friedrich, MG, Heberle, J, Naumann, RL & Knoll, W (2004) The protein-tethered lipid bilayer: A novel mimic of the biological membrane. Biophys J 87, 3213-3220.
[2] Ataka, K, Giess, F, Knoll, W, Naumann, R, Haber-Pohlmeier, S, Richter, B & Heberle, J (2004) Oriented attachment and membrane reconstitution of his-tagged cytochrome c oxidase to a gold electrode: In situ monitoring by surface-enhanced infrared absorption spectroscopy. J Am Chem Soc 126, 16199-16206.
[3] Grosserueschkamp, M, Nowak, C, Schach, D, Schaertl, W, Knoll, W & Naumann, RLC (2009) Silver Surfaces with Optimized Surface Enhancement by Self-Assembly of Silver Nanoparticles for Spectroelectrochemical Applications. J Phys Chem C 113, 17698-17704.
[4] Nowak, C, Santonicola, MG, Schach, D, Zhu, J, Gennis, RB, Ferguson-Miller, S, Baurecht, D, Walz, D, Knoll, W & Naumann, RLC (2010) Conformational transitions and molecular hysteresis of cytochrome c oxidase: Varying the redox state by electronic wiring. Soft Matter 6, 5523-5532.
[5] Schwaighofer, A, Steininger, C, Hildenbrandt, David M, Srajer, J, Nowak, C, Knoll, W & Naumann, Renate LC (2013) Time-Resolved Surface-Enhanced IR-Absorption Spectroscopy of Direct Electron Transfer to Cytochrome c Oxidase from R. sphaeroides. Biophys J 105, 2706-2713.
[6] Steininger, C, Reiner-Rozman, C, Schwaighofer, A, Knoll, W & Naumann, RL (2016) Kinetics of cytochrome c oxidase from R. sphaeroides initiated by direct electron transfer followed by tr-SEIRAS. Bioelectrochemistry 112, 1-8.
[7] Schwaighofer, A, Ferguson-Miller, S, Naumann, RLC, Knoll, W & Nowak, C (2014) Phase-Sensitive Detection in Modulation Excitation Spectroscopy Applied to Potential Induced Electron Transfer in Cytochrome c Oxidase. Appl Spectrosc 68, 5-13.
[8] Jiang, X, Zaitseva, E, Schmidt, M, Siebert, F, Engelhard, M, Schlesinger, R, Ataka, K, Vogel, R & Heberle, J (2008) Resolving voltage-dependent structural changes of a membrane photoreceptor by surface-enhanced IR difference spectroscopy. Proc Natl Acad Sci 105, 12113-12117.
[9] Nedelkovski, V, Schwaighofer, A, Wraight, C, Nowak, C & Naumann, RLC (2013) Surface-Enhanced Infrared Absorption Spectroscopy (SEIRAS) of Light-Activated Photosynthetic Reaction Centers from Rhodobacter sphaeroides Reconstituted in a Biomimetic Membrane System. J Phys Chem C 117, 16357−16363.
[10] Shinkarev, VP, Ugulava, NB, Takahashi, E, Crofts, AR & Wraight, CA (2000) Aspartate-187 of cytochrome b is not needed for DCCD inhibition of ubiquinol: Cytochrome c oxidoreductase in Rhodobacter sphaeroides chromatophores. Biochemistry 39, 14232-14237.
[11] Shinkarev, VP, Crofts, AR & Wraight, CA (2001) The electric field generated by photosynthetic reaction center induces rapid reversed electron transfer in the bc(1) complex. Biochemistry 40, 12584-12590.
[12] Breton, J (2007) Steady-state FTIR spectra of the photoreduction of Q(A) and Q(B) in Rhodobacter sphaeroides reaction centers provide evidence against the presence of a proposed transient electron acceptor X between the two quinones. Biochemistry 46, 4459-4465.
[13] Brudler, R & Gerwert, K (1998) Step-scan FTIR spectroscopy resolves the Q(A)(-)Q(B)-> Q(A)Q(B)(-) transition in Rb-sphaeroides R26 reaction centres. Photosynth Res 55, 261-266.
[14] Iwata, T, Paddock, ML, Okamura, MY & Kandori, H (2009) Identification of FTIR Bands Due to Internal Water Molecules around the Quinone Binding Sites in the Reaction Center from Rhodobacter sphaeroides. Biochemistry 48, 1220-1229.
[15] Mezzetti, A, Blanchet, L, de Juan, A, Leibl, W & Ruckebusch, C (2011) Ubiquinol formation in isolated photosynthetic reaction centres monitored by time-resolved differential FTIR in combination with 2D correlation spectroscopy and multivariate curve resolution. Anal Bioanal Chem 399, 1999-2014.
[16] Nabedryk, E & Breton, J (2008) Coupling of electron transfer to proton uptake at the QB site of the bacterial reaction center: A perspective from FTIR difference spectroscopy. Biochim Biophys Acta, Bioenerg 1777, 1229-1248.
[17] Nowak, C, Luening, C, Knoll, W & Naumann, RLC (2009) A Two-Layer Gold Surface with Improved Surface Enhancement for Spectro-Electrochemistry Using Surface-Enhanced Infrared Absorption Spectroscopy. Appl Spectrosc 63, 1068-1074.
[18] Hielscher, R, Wenz, T, Hunte, C & Hellwig, P (2009) Monitoring the redox and protonation dependent contributions of cardiolipin in electrochemically induced FTIR difference spectra of the cytochrome bc(1) complex from yeast. Biochim Biophys Acta, Bioenerg 1787, 617-625.
[19] Ritter, M, Anderka, O, Ludwig, B, Mantele, W & Hellwig, P (2003) Electrochemical and FTIR spectroscopic characterization of the cytochrome bc(1) complex from Paracoccus denitrificans: Evidence for protonation reactions coupled to quinone binding. Biochemistry 42, 12391-12399.
[20] Iwaki, M, Giotta, L, Akinsiku, AO, H., S, Fisher, N, Breton, J & Rich, P (2003) Redox-Induced Transitions in Bovine Cytochrome bc Complex Studied by Perfusion-Induced ATR-FTIR Spectroscopy. Biochemistry 42, 11109-11119.
[21] Nowak, C, Laredo, T, Lipkowski, J, Gennis, RB, Ferguson-Miller, S, Knoll, W & Naumann, RLC (2011) 2D-SEIRA spectroscopy to highlight Conformational Changes of the Cytochrome c Oxidase induced by direct electron transfer, Metallomics, 2011, 3 (6), 619 - 627. Metallomics 3, 619-627.
[22] Osawa, M (2001) Surface-enhanced Infrared Absorption Spectroscopy in Near Field Optics and Surface Plasmon Polaritons (Kawata, S., ed) pp. 163-184, Springer, Berlin/Heidelberg.
[23] Leonhard, M & Mantele, W (1993) Fourier transform infrared spectroscopy and electrochemistry of the primary electron donor in Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction centers: vibrational modes of the pigments in situ and evidence for protein and water modes affected by P+ formation. Biochemistry 32, 4532-4538.
[24] Breton, J & Nabedryk, E (1996) Protein-quinone interactions in the bacterial photosynthetic reaction center: Light-induced FTIR difference spectroscopy of the quinone vibrations. Biochim Biophys Acta, Bioenerg 1275, 84-90.
[25] Remy, A & Gerwert, K (2003) Coupling of light-induced electron transfer to proton uptake in photosynthesis. Nat Struct Biol 10, 637-644.
[26] Breton, J, Thibodeau, DL, Berthomieu, C, Mantele, W, Vermeglio, A & Nabedryk, E (1991) Probing the primary quinone environment in photosynthetic bacterial reaction centers by light-induced FTIR difference spectroscopy. FEBS Lett 278, 257-260.
[27] Stuart, B (1997) Biological Applications of Infrared Spectroscopy, John Wiley & Sons, Ltd.
[28] Mezzetti, A & Leibl, W (2005) Investigation of ubiquinol formation in isolated photosynthetic reaction centers by rapid-scan Fourier transform IR spectroscopy. Eur Biophys J 34, 921-936.
[29] Kirmaier, C, Laible, PD, Czarnecki, K, Hata, AN, Hanson, DK, Bocian, DF & Holten, D (2002) Comparison of M-side electron transfer in Rb. sphaeroides and Rb. capsulatus reaction centers. J Phys Chem B 106, 1799-1808.
[30] Breton, J, Boullais, C, Burie, JR, Nabedryk, E & Mioskowski, C (1994) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: assignment of the interactions of each carbonyl of QA in Rhodobacter sphaeroides using site-specific 13C-labeled ubiquinone. Biochemistry 33, 14378-14386.
[31] Breton, J, Boullais, C, Berger, G, Mioskowski, C & Nabedryk, E (1995) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: symmetry of the carbonyl interactions and close equivalence of the QB vibrations in Rhodobacter sphaeroides and Rhodopseudomonas viridis probed by isotope labeling. Biochemistry 34, 11606-11616.
[32] Mäntele, W, Nabedryk, E, Tavitian, BA, Kreutz, W & Breton, J (1985) Light-induced Fourier transform infrared (FTIR) spectroscopic investigations of the primary donor oxidation in bacterial photosynthesis. FEBS Lett 187, 227-232.
[33] Mezzetti, A, Blanchet, L, Juan, A, Leibl, W & Ruckebusch, C (2011) Ubiquinol formation in isolated photosynthetic reaction centres monitored by time-resolved differential FTIR in combination with 2D correlation spectroscopy and multivariate curve resolution. Anal Bioanal Chem 399, 1999-2014.
[34] Mezzetti, A, Leibl, W, Breton, J & Nabedryk, E (2003) Photoreduction of the quinone pool in the bacterial photosynthetic membrane: identification of infrared marker bands for quinol formation. FEBS Lett 537, 161-165.
[35] Wraight, CA (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front Biosci, Landmark Ed 9, 309-337.
[36] Fato, R, Battino, M, Degli Esposti, M, Parenti Castelli, G & Lenaz, G (1986) Determination of partition and lateral diffusion coefficients of ubiquinones by fluorescence quenching of n-(9-anthroyloxy) stearic acids in phospholipid vesicles and mitochondrial membranes. Biochemistry 25, 3378-3390.
[37] Crofts, AR, Holland, JT, Victoria, D, Kolling, DRJ, Dikanov, SA, Gilbreth, R, Lhee, S, Kuras, R & Kuras, MG (2008) The Q-cycle reviewed: How well does a monomeric mechanism of the bc(1) complex account for the function of a dimeric complex? Biochim Biophys Acta, Bioenerg 1777, 1001-1019.
[38] Chobot, SE, Zhang, H, Moser, CC & Dutton, PL (2008) Breaking the Q-cycle. finding new ways to stuidy Q0 through thermodynamic calculations. J Bioenerg Biomembr, 501-507.
[39] Mulkidjanian, A (2005) Ubiquinol oxidation in the cytochrome bc1 complex: Reaction mechanism and prevention of short-circuiting Biochim Biophys Acta 1709, 5-34.
[40] Snyder, CH & Trumpower, BL (1999) Ubiquinone at Center N Is Responsible for Triphasic Reduction of Cytochrome b in the Cytochromebc 1 Complex. J Biol Chem 274, 31209-31216.
[41] Iwaki, M, Osyczka, A, Moser, C, Dutton, PL & Rich, P (2004) ATR-FTIR Spectrocopy Studies of iron–sulfur protein and cytochrome in the Rhodobacter capsulatus Cytochrome bc Complex Biochemistry 43, 9477-9486.
[42] Goldsmith, JO & Boxer, SG (1996) Rapid isolation of bacterial photosynthetic reaction centers with an engineered poly-histidine tag. Biochim Biophys Acta, Bioenerg 1276, 171-175.
[43] Guergova-Kuras, M, Salcedo-Hernandez, R, Bechmann, G, Kuras, R, Gennis, RB & Crofts, AR (1999) Expression and one-step purification of a fully active polyhistidine-tagged cytochrome bc(1) complex from Rhodobacter sphaeroides. Protein Expression Purif 15, 370-380.
Author Information
  • Austrian Institute of Technology GmbH, Vienna, Austria

  • Austrian Institute of Technology GmbH, Vienna, Austria; Institute of Chemical Technologies and Analytics, Vienna University of Technology, Vienna, Austria

  • Austrian Institute of Technology GmbH, Vienna, Austria

  • Institute of Chemical Technologies and Analytics, Vienna University of Technology, Vienna, Austria; Center of Electrochemical Surface Technology, Wiener Neustadt, Austria

  • Austrian Institute of Technology GmbH, Vienna, Austria

Cite This Article
  • APA Style

    Vedran Nedelkovski, Andreas Schwaighofer, Andreas F. Geiss, Christina Bliem, Renate L. C. Naumann. (2017). Interactions of Photosynthetic Reaction Centers with Bc1 Complexes from Rhodobacter Sphaeroides Studied Using SEIRAS on a Nano-Structured Gold Surface. International Journal of Bioorganic Chemistry, 2(2), 61-69. https://doi.org/10.11648/j.ijbc.20170202.13

    Copy | Download

    ACS Style

    Vedran Nedelkovski; Andreas Schwaighofer; Andreas F. Geiss; Christina Bliem; Renate L. C. Naumann. Interactions of Photosynthetic Reaction Centers with Bc1 Complexes from Rhodobacter Sphaeroides Studied Using SEIRAS on a Nano-Structured Gold Surface. Int. J. Bioorg. Chem. 2017, 2(2), 61-69. doi: 10.11648/j.ijbc.20170202.13

    Copy | Download

    AMA Style

    Vedran Nedelkovski, Andreas Schwaighofer, Andreas F. Geiss, Christina Bliem, Renate L. C. Naumann. Interactions of Photosynthetic Reaction Centers with Bc1 Complexes from Rhodobacter Sphaeroides Studied Using SEIRAS on a Nano-Structured Gold Surface. Int J Bioorg Chem. 2017;2(2):61-69. doi: 10.11648/j.ijbc.20170202.13

    Copy | Download

  • @article{10.11648/j.ijbc.20170202.13,
      author = {Vedran Nedelkovski and Andreas Schwaighofer and Andreas F. Geiss and Christina Bliem and Renate L. C. Naumann},
      title = {Interactions of Photosynthetic Reaction Centers with Bc1 Complexes from Rhodobacter Sphaeroides Studied Using SEIRAS on a Nano-Structured Gold Surface},
      journal = {International Journal of Bioorganic Chemistry},
      volume = {2},
      number = {2},
      pages = {61-69},
      doi = {10.11648/j.ijbc.20170202.13},
      url = {https://doi.org/10.11648/j.ijbc.20170202.13},
      eprint = {https://download.sciencepg.com/pdf/10.11648.j.ijbc.20170202.13},
      abstract = {Inter-protein reactions of photosynthetic reaction centers (RCs) with bc1 complexes from R. sphaeroides, have been investigated using surface-enhanced Infrared-absorption spectroscopy (SEIRAS). Surface enhancement was achieved by a nano-structured gold surface. The proteins were immobilized via his-tags attached to the P side of the RC and the C-terminal end of the cytochrome (cyt) b subunit and co-reconstituted into a lipid bilayer by in-situ dialysis. In this configuration, the cyt c binding site of the two proteins is located on opposite sides of the membrane. Light-minus-dark absorbance spectra under continuous illumination in the absence of an electron donor indicated a slow quinone/semiquinone exchange, allowing release of ubiquinol (QH2) into the membrane. The interaction of the bc1 with QH2 was indicated by the stationary state obtained but only in the presence of cyt c. The interaction is discussed in terms of a semiquinone species formed in the course of the Q cycle mechanism of the bc1.},
     year = {2017}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Interactions of Photosynthetic Reaction Centers with Bc1 Complexes from Rhodobacter Sphaeroides Studied Using SEIRAS on a Nano-Structured Gold Surface
    AU  - Vedran Nedelkovski
    AU  - Andreas Schwaighofer
    AU  - Andreas F. Geiss
    AU  - Christina Bliem
    AU  - Renate L. C. Naumann
    Y1  - 2017/03/22
    PY  - 2017
    N1  - https://doi.org/10.11648/j.ijbc.20170202.13
    DO  - 10.11648/j.ijbc.20170202.13
    T2  - International Journal of Bioorganic Chemistry
    JF  - International Journal of Bioorganic Chemistry
    JO  - International Journal of Bioorganic Chemistry
    SP  - 61
    EP  - 69
    PB  - Science Publishing Group
    SN  - 2578-9392
    UR  - https://doi.org/10.11648/j.ijbc.20170202.13
    AB  - Inter-protein reactions of photosynthetic reaction centers (RCs) with bc1 complexes from R. sphaeroides, have been investigated using surface-enhanced Infrared-absorption spectroscopy (SEIRAS). Surface enhancement was achieved by a nano-structured gold surface. The proteins were immobilized via his-tags attached to the P side of the RC and the C-terminal end of the cytochrome (cyt) b subunit and co-reconstituted into a lipid bilayer by in-situ dialysis. In this configuration, the cyt c binding site of the two proteins is located on opposite sides of the membrane. Light-minus-dark absorbance spectra under continuous illumination in the absence of an electron donor indicated a slow quinone/semiquinone exchange, allowing release of ubiquinol (QH2) into the membrane. The interaction of the bc1 with QH2 was indicated by the stationary state obtained but only in the presence of cyt c. The interaction is discussed in terms of a semiquinone species formed in the course of the Q cycle mechanism of the bc1.
    VL  - 2
    IS  - 2
    ER  - 

    Copy | Download

  • Sections