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Modulating the lifetime of the charge-separated state in photosynthetic reaction center by out-of-protein electrostatics

Published online by Cambridge University Press:  01 March 2018

Francesco Milano
Affiliation:
CNR-IPCF, Istituto per i Processi Chimico Fisici – Consiglio Nazionale delle Ricerche – Via Orabona, 4 – 70125 BARI.
Roberto R. Tangorra
Affiliation:
Departmento of Chemistry – Università degli Studi di Bari, Via Orabona, 4 – 70125 BARI.
Angela Agostiano
Affiliation:
CNR-IPCF, Istituto per i Processi Chimico Fisici – Consiglio Nazionale delle Ricerche – Via Orabona, 4 – 70125 BARI. Departmento of Chemistry – Università degli Studi di Bari, Via Orabona, 4 – 70125 BARI.
Livia Giotta
Affiliation:
DiSTeBA Department of Biology and Environmental Science and Technology – Università del Salento, Via Provinciale Lecce Monteroni 165, I-73100 Lecce, Italy.
Vincenzo De Leo
Affiliation:
Departmento of Chemistry – Università degli Studi di Bari, Via Orabona, 4 – 70125 BARI.
Fulvio Ciriaco
Affiliation:
Departmento of Chemistry – Università degli Studi di Bari, Via Orabona, 4 – 70125 BARI.
Massimo Trotta*
Affiliation:
CNR-IPCF, Istituto per i Processi Chimico Fisici – Consiglio Nazionale delle Ricerche – Via Orabona, 4 – 70125 BARI.
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Abstract

The photosynthetic reaction center (RC) is an integral membrane protein that, upon absorption of photons, generates a hole-electron couple with a yield close to one. This energetic state has numerous possible applications in several biotechnological fields given that its lifetime is long enough to allow non-metabolic ancillary redox chemistry to take place. Here we focus on RCs reconstituted in liposomes, formed with sole phospholipids or in blends with other lipids, and show that the electrical charge sitting on the polar head of such hydrophobic molecules does play an important role on the stability of the hole-electron couple. More specifically this study shows that the presence of negative charges in the surrounding of the protein stabilizes the charge-separated state while positive charges have a strong opposite effect.

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Copyright © Materials Research Society 2018 

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Footnotes

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Present address: Mossi & Ghisolfi Group, strada Ribrocca 11 - 15057 Tortona, Italy

References

Tangorra, R.R., et al. ., Hybrid Interfaces for Electron and Energy Transfer Based on Photosynthetic Proteins, in Handbook of Photosynthesis, Third Edition, Pessarakli, M., Editor. 2016, CRC Press. p. 201220.Google Scholar
Maróti, P. and Trotta, M., Artificial Photosynthetic Systems, in CRC Handbook of Organic Photochemistry and Photobiology, Third Edition - Two Volume Set, Griesbeck, A., Oelgemöller, M., and Ghetti, F., Editors. 2012, CRC Press. p. 12891324.Google Scholar
Cardona, T., A fresh look at the evolution and diversification of photochemical reaction centers. Photosynthesis Research, 2015. 126(1): p. 111134.Google Scholar
Gisriel, C., et al. ., Structure of a symmetric photosynthetic reaction center–photosystem. Science, 2017.CrossRefGoogle ScholarPubMed
Venturoli, G., et al. ., Temperature dependence of charge recombination from the P+QA- abd P+QB- states in photosynthetic reaction centres isolated from thermophilic bacterium Chloroflexus aurantiacus. Eur. J. Biochem., 1991. 202: p. 625634.Google Scholar
Zabelin, A.A., et al. ., FTIR Spectroscopy of the Reaction Center of Chloroflexus aurantiacus: Photooxidation of the Primary Electron Donor. Biochemistry-Moscow, 2012. 77(2): p. 157164.Google Scholar
Feher, G., et al. ., Structure and function of bacterial photosynthetic reaction centres. Nature, 1989. 339: p. 111116.Google Scholar
Deisenhofer, J. and Michel, H., The Photosynthetic Reaction Center from the Purple Bacterium Rhodopseudomonas viridis. Science, 1989. 245(4925): p. 1463–73.Google Scholar
Singer, S.J. and Nicolson, G.L., The Fluid Mosaic Model of the Structure of Cell Membranes. Science, 1972. 175(4023): p. 720.Google Scholar
Allen, J.P., et al. ., Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proceedings of the National Academy of Sciences, 1987. 84(17): p. 61626166.CrossRefGoogle ScholarPubMed
Allen, J.P., et al. ., Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proceedings of the National Academy of Sciences, 1987. 84(16): p. 57305734.Google Scholar
Yeates, T.O., et al. ., Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1: protein-cofactor (bacteriochlorophyll, bacteriopheophytin, and carotenoid) interactions. Proceedings of the National Academy of Sciences, 1988. 85(21): p. 79937997.Google Scholar
Allen, J.P., et al. ., Structure of the reaction center from Rhodobacter sphaeroides R-26: protein-cofactor (quinones and Fe2+) interactions. Proceedings of the National Academy of Sciences, 1988. 85(22): p. 84878491.Google Scholar
Koepke, J., et al. ., pH Modulates the Quinone Position in the Photosynthetic Reaction Center from Rhodobacter sphaeroides in the Neutral and Charge Separated States. Journal of Molecular Biology, 2007. 371(2): p. 396409.Google Scholar
Peluso, A., et al. ., A plausible mechanism of electron transfer between quinones in photosynthetic reaction centers. J Theor Biol, 2000. 207(1): p. 101–5.CrossRefGoogle Scholar
Di Donato, M., Peluso, A., and Villani, G., Electron Transfer between Quinones in Photosynthetic Reaction Centers. The Journal of Physical Chemistry B, 2004. 108(9): p. 30683077.Google Scholar
Kressel, L., et al. ., High yield of secondary B-side electron transfer in mutant Rhodobacter capsulatus reaction centers. Biochim Biophys Acta, 2014. 1837(11): p. 1892–903.CrossRefGoogle ScholarPubMed
Kleinfeld, D., Okamura, M.Y., and Feher, G., Electron transfer in reaction centers of Rhodopseudomonas sphaeroides. II. Free energy and kinetic relations between the acceptor states QA−QB− and QAQ2−B. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1985. 809(3): p. 291310.Google Scholar
Kleinfeld, D., Okamura, M.Y., and Feher, G., Electron transfer in reaction centers of Rhodopseudomonas sphaeroides. I. Determination of the charge recombination pathway of D+QAQ−B and free energy and kinetic relations between Q−AQB and QAQ−B. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1984. 766(1): p. 126140.Google Scholar
Warncke, K. and Dutton, P.L., Influence of Q(a)-Site Redox Cofactor Structure on Equilibrium Binding, Insitu Electrochemistry, and Electron-Transfer Performance in the Photosynthetic Reaction Center Protein. Biochemistry, 1993. 32(18): p. 47694779.Google Scholar
Giangiacomo, K.M., Gunner, M.R., and Dutton, P.L., Qa and Qb Site Control of Quinone Electrochemistry in the Photosynthetic Reaction Center from Rhodobacter-Sphaeroides. Biophysical Journal, 1990. 57(2): p. A566-A566.Google Scholar
Maroti, P., Kinetics and yields of bacteriochlorophyll fluorescence: redox and conformation changes in reaction center of Rhodobacter sphaeroides. European Biophysics Journal with Biophysics Letters, 2008. 37(7): p. 11751184.CrossRefGoogle ScholarPubMed
Turzo, K., et al. ., Quinone-dependent delayed fluorescence from the reaction center of photosynthetic bacteria. Biophysical Journal, 2000. 79(1): p. 1425.Google Scholar
Emese, A., et al. ., The reaction center is the sensitive target of the mercury(II) ion in intact cells of photosynthetic bacteria. Photosynthesis Research, 2012. 112(2): p. 129140.Google Scholar
Kleinfeld, D., Okamura, M.Y., and Feher, G., Charge recombination kinetics as a probe of protonation of the primary acceptor in photosynthetic reaction centers. Biophys J, 1985. 48(5): p. 849–52.Google Scholar
Kim, I., et al. ., Modeling gating charge and voltage changes in response to charge separation in membrane proteins. Proc Natl Acad Sci U S A, 2014. 111(31): p. 11353–8.CrossRefGoogle ScholarPubMed
Li, L., et al. ., On the Dielectric “Constant” of Proteins: Smooth Dielectric Function for Macromolecular Modeling and Its Implementation in DelPhi. Journal of Chemical Theory and Computation, 2013. 9(4): p. 21262136.Google Scholar
Agostiano, A., Milano, F., and Trotta, M., Investigation on the detergent role in the function of secondary quinone in bacterial reaction centers. European Journal of Biochemistry, 1999. 262(2): p. 358364.Google Scholar
Milano, F., et al. ., Characterisation of RC-proteoliposomes at different RC/lipid ratios. Photosynthesis research, 2009. 100(2): p. 107–12.Google Scholar
Muh, F., Rautter, J., and Lubitz, W., Effects of zwitterionic detergents on the primary donor of bacterial reaction centers. Berichte Der Bunsen-Gesellschaft-Physical Chemistry Chemical Physics, 1996. 100(12): p. 19741977.Google Scholar
Muh, F., Rautter, J., and Lubitz, W., Two distinct conformations of the primary electron donor in reaction centers from Rhodobacter sphaeroides revealed by ENDOR/TRIPLE-spectroscopy. Biochemistry, 1997. 36(14): p. 4155–62.CrossRefGoogle ScholarPubMed
Trotta, M., et al. ., Response of membrane protein to the environment: the case of photosynthetic Reaction Centre. Materials Science & Engineering. C, Biomimetic and Supramolecular Systems, 2002. 22(2): p. 263267.Google Scholar
Agostiano, A., et al. ., Charge recombination of photosynthetic reaction centres in different membrane models. Gazzetta Chimica Italiana, 1995. 125: p. 615622.Google Scholar
Overfield, R.E. and Wraight, C.A., Oxidation of cytochromes c and c2 by bacterial photosynthetic reaction centers in phospholipid vesicles. 1. Studies with neutral membranes. Biochemistry, 1980. 19(14): p. 3322–7.Google Scholar
Overfield, R.E. and Wraight, C.A., Oxidation of cytochromes c and c2 by bacterial photosynthetic reaction centers in phospholipid vesicles. 2. Studies with negative membranes. Biochemistry, 1980. 19(14): p. 3328–34.Google Scholar
Agostiano, A., et al. ., pH-sensitive fluorescent dye as probe for proton uptake in photosynthetic reaction centers. Bioelectrochemistry, 2004. 63(1-2): p. 125–8.Google Scholar
Nagy, L., et al. ., Protein/lipid interaction in the bacterial photosynthetic reaction center: Phosphatidylcholine and phosphatidylglycerol modify the free energy levels of the quinones. Biochemistry, 2004. 43(40): p. 1291312923.CrossRefGoogle ScholarPubMed
Trotta, M., et al. ., Protein/lipid interaction in bacterial photosynthetic reaction center: the role of phosphatidylcholine and phosphatidylglycerol in charge stabilization. Biochimica Et Biophysica Acta-Bioenergetics, 2004. 1658: p. 263–263.Google Scholar
Isaacson, R.A., et al. ., Electronic structure of Q-A in reaction centers from Rhodobacter sphaeroides. I. Electron paramagnetic resonance in single crystals. Biophysical Journal, 1995. 69(2): p. 311–22.Google Scholar
Milano, F., et al. ., Kinetics of the quinone binding reaction at the Q(B) site of reaction centers from the purple bacteria Rhodobacter sphaeroides reconstituted in liposomes. European Journal of Biochemistry, 2003. 270(23): p. 45954605.Google Scholar
Almog, S., et al. ., Kinetic and structural aspects of reconstitution of phosphatidylcholine vesicles by dilution of phosphatidylcholine-sodium cholate mixed micelles. Biochemistry, 1986. 25(9): p. 2597–605.Google Scholar
Milano, F., et al. ., Enhancing the Light Harvesting Capability of a Photosynthetic Reaction Center by a Tailored Molecular Fluorophore. Angewandte Chemie, 2012. 124(44): p. 1118111185.Google Scholar
McAuley, K.E., et al. ., Structural details of an interaction between cardiolipin and an integral membrane protein. Proc Natl Acad Sci U S A, 1999. 96(26): p. 14706–11.Google Scholar
Catucci, L., et al. ., Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochemistry, 2004. 43(47): p. 1506615072.Google Scholar
Rinyu, L., et al. ., Modulation of the free energy of the primary quinone acceptor (QA) in Reaction Centers from Rhodobacter sphaeroides: Contribution from the protein and the protein-lipid (cardiolipin) interactions. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2004. 1655: p. 93101.Google Scholar
Dezi, M., et al. ., Stabilization of charge separation and cardiolipin confinement in antenna-reaction center complexes purified from Rhodobacter sphaeroides. Biochimica Et Biophysica Acta-Bioenergetics, 2007. 1767(8): p. 10411056.Google Scholar
De Leo, V., et al. ., Cardiolipin increases in chromatophores isolated from Rhodobacter sphaeroides after osmotic stress: structural and functional roles. Journal of Lipid Research, 2009. 50(2): p. 256264.CrossRefGoogle ScholarPubMed
Catucci, L., et al. ., Oxidoreductase activity of chromatophores and purified cytochrome bc (1) complex from Rhodobacter sphaeroides: a possible role of cardiolipin. Journal of Bioenergetics and Biomembranes, 2012. 44(4): p. 487493.Google Scholar
Wydro, P., The influence of cardiolipin on phosphatidylglycerol/phosphatidylethanolamine monolayers—Studies on ternary films imitating bacterial membranes. Colloids and Surfaces B: Biointerfaces, 2013. 106: p. 217223.Google Scholar
Operamolla, A., et al. ., “Garnishing” the photosynthetic bacterial reaction center for bioelectronics. Journal of Materials Chemistry C, 2015. 3(25): p. 64716478.Google Scholar
De Leo, V., et al. ., Effect of ultrasound on the function and structure of a membrane protein: The case study of photosynthetic Reaction Center from Rhodobacter sphaeroides. Ultrasonics Sonochemistry, 2017. 35: p. 103111.Google Scholar
Swainsbury, D.J., et al. ., Evaluation of a biohybrid photoelectrochemical cell employing the purple bacterial reaction centre as a biosensor for herbicides. Biosens Bioelectron, 2014. 58: p. 172–8.CrossRefGoogle ScholarPubMed
Swainsbury, D.J., et al. ., Directed assembly of defined oligomeric photosynthetic reaction centres through adaptation with programmable extra-membrane coiled-coil interfaces. Biochim Biophys Acta, 2016. 1857(12): p. 18291839.CrossRefGoogle ScholarPubMed
Tangorra, R.R., et al. ., Assembly of a photosynthetic reaction center with ABA tri-block polymersomes: highlights on protein localization. Photochemical & Photobiological Sciences, 2015. 14(10): p. 18441852.Google Scholar
Milano, F., et al. ., Functional Enzymes in Nonaqueous Environment: The Case of Photosynthetic Reaction Centers in Deep Eutectic Solvents. ACS Sustainable Chemistry & Engineering, 2017. 5(9): p. 77687776.Google Scholar
Hassan Omar, O., et al. ., Synthetic Antenna Functioning As Light Harvester in the Whole Visible Region for Enhanced Hybrid Photosynthetic Reaction Centers. Bioconjugate Chemistry, 2016. 27(7): p. 16141623.Google Scholar
la Gatta, S., et al. ., A far-red emitting aryleneethynylene fluorophore used as light harvesting antenna in hybrid assembly with the photosynthetic reaction center. MRS Advances, 2016. 1(7): p. 495500.CrossRefGoogle Scholar
Dutta, P.K., et al. ., Reengineering the optical absorption cross-section of photosynthetic reaction centers. J Am Chem Soc, 2014. 136(12): p. 4599–604.CrossRefGoogle ScholarPubMed
Dutta, P.K., et al. ., A DNA-Directed Light-Harvesting/Reaction Center System. Journal of the American Chemical Society, 2014. 136(47): p. 1661816625.Google Scholar