Abstract
Semiquinone oscillations induced by light pulses in the presence of exogenous electron donors are a valuable source of information on the kinetics and thermodynamics of ubiquinone chemistry relevant to the QB site of the photosynthetic reaction center (RC). In previous attempts to achieve the quantitative interpretation of data, the ubiquinone concentration was considered constant during the experiment since it was much bigger than that of RC. In this work, we extended existing models to low ubiquinone concentrations revealing several hidden processes taking place during the ubiquinone photoreduction and enabling the evaluation of the ubiquinone binding constant K Q at the QB site. The proposed approach provides for the first time the evaluation of K Q without any preliminary treatment of ubiquinone extraction from the binding site, thereby better preserving its native structure.
Similar content being viewed by others
References
Agostiano A, Milano F, Trotta M (1999) Investigation on the detergent role in the function of secondary quinone in bacterial reaction centers. Eur J Biochem 262:358–364
Bowyer JR, Meinhardt SW, Tierney GV, Crofts AR (1981) Resolved difference spectra of redox centers involved in photosynthetic electron flow in Rhodopseudomonas capsulata and Rhodopseudomonas sphaeroides. Biochim Biophys Acta 635:167–186
Feher G, Allen JP, Okamura MY, Rees DC (1989) Structure and function of bacterial photosynthetic reaction centres. Nature 339:111–116
Georges J, Desmettre S (1984) Electrochemistry of ferrocene in anionic, cationic and nonionic micellar solutions. Effet of the micelle solubilization of the half-wave potentials. Electrochim Acta 29:521–525
Halmschlager A, Trotta M, Tandori JL, Trotta M, Rinyu L, Pfeiffer I, Nagy L (2002) A mathematical model for quinone–herbicide competition in the reaction centres of Rhodobacter sphaeroides. Funct Plant Biol 29:443–449
Kleinfeld D, Abresch EC, Okamura MY, Feher G (1984) Damping of oscillations in the semiquinone absorption in reaction centres after succesive flashes. Biochim Biophys Acta 765:406–409
Kleinfeld D, Okamura MY, Fcher G (1985) Electron transfer in reaction centers of Rhodopseudomonas sphaeroides. II. Free energy and kinetic relations between the acceptor states Q(-)A Q(-)B and QAQ(2-)B. Biochim Biophys Acta 809:291–310
Mallardi A, Palazzo G, Venturoli G (1997) Binding of ubiquinone to photosynthetic reaction centers: determination of enthalpy and entropy changes in reverse micelles. J Phys Chem B 101:7850–7857
Maróti P, Wraight CA (1988) Flash-induced H+ binding by bacterial photosynthetic reaction centers: comparison of spectrophotometric and conductimetric methods. Biochim Biophys Acta (BBA) 934:314–328
Mavelli F, Trotta M, Ciriaco F, Agostiano A, Giotta L, Italiano F, Milano F (2014) The binding of quinone to the photosynthetic reaction centers: kinetics and thermodynamics of reactions occurring at the Q(B)-site in zwitterionic and anionic liposomes. Eur Biophys J Biophy 43:301–315
McComb JC, Stein RR, Wraight CA (1990) Investigations on the influence of headgroup substitution and isoprene side-chain length in the function of primary and secondary quinones of bacterial reaction centers. Biochim Biophys Acta 1015:156–171
Milano F, Agostiano A, Mavelli F, Trotta M (2003) Kinetics of the quinone binding reaction at the QB site of reaction centers from the purple bacteria Rhodobacter sphaeroides reconstituted in liposomes. Eur J Biochem 270:4595–4605
Milano F, Gerencser L, Agostiano A, Nagy L, Trotta M, Maroti P (2007) Mechanism of quinol oxidation by ferricenium produced by light excitation in reaction centers of photosynthetic bacteria. J Phys Chem B 111:4261–4270
Milano F, Altamura E, Agostiano A, Giotta L, Trotta M (2008) Spectral and kinetic properties of semiquinones in bacterial photosynthetic reaction centres embedded in liposomes obtained by different phospholipds. In: Allen J, Gantt E, Goldbeck J, Osmond B (eds) Photosynthesis Energy from the sun, vol 2. Springer, Dordrecht, pp 141–144
Milano F, Italiano F, Agostiano A, Trotta M (2009) Characterisation of RC-proteoliposomes at different RC/lipid ratios. Photosynth Res 100:107–112
Milioto S, Romancino D, De Lisi R (1987) Excess enthalpies of solution of primary and secondary alcohols in dodecyldimethylamine oxide micellar solutions. J Solut Chem 16:943–956
Okamura MY, Isaacson RA, Feher G (1975) The primary acceptor in bacterial photosynthesis: the obligatory role of ubiquinone in photoactive reaction centres of Rp. sphaeroides. Proc Natl Acad Sci USA 72:3491–3495
Roth M, Lewit-Bentley A, Michel H, Deisenhofer J, Huber R, Oesterhelt D (1989) Detergent structure in crystals of a bacterial photosynthetic reaction centre. Nature 340:659–662
Shinkarev VP (1998) The general kinetic model of electron transfer in photosynthetic reaction centers activated by multiple flashes. Photochem Photobiol 67:683–699
Shinkarev VP, Wraight CA (1993) Electron and proton transfer in the acceptor quinone complex of reaction centres of phototrophic bacteria. In: Deisenhofer J, Norris JR (eds) The photosynthetic reaction center. Academic Press, San Diego, pp 193–255
Shinkarev VP, Wraight CA (1997a) The interaction of quinone and detergent with reaction centers of purple bacteria.I. Slow quinone exchange between reaction center micelles and pure detergent micelles. Biophys J 72:2304–2319
Shinkarev VP, Wraight CA (1997b) The interaction of quinone and detergent with reaction centers of purple bacteria. I. Slow quinone exchange between reaction center micelles and pure detergent micelles. Biophys J 72:2304–2319
Tandori J, Nagy L, Maróti P (1991) Semiquinone oscillation as a probe of quinone/herbicide binding in bacterial reaction centers. Photosynthetica 25:7
Vermeglio A (1977) Secondary electron transfer in reaction centers of Rhodopseudomonas sphaeroides. Out-of-phase periodicity of two for the formation of ubisemiquinone and fully reduced ubiquinone. Biochim Biophys Acta 459:516–524
Vermeglio A, Clayton RK (1977) Kinetics of electron transfer between the primary and the secondary electron acceptor in reaction centers from Rhodopseudomonas sphaeroides. Biochim Biophys Acta (BBA) Bioenerg 461:159–165
Wraight CA (1977) Electron acceptors of photosynthetic bacterial reaction centers. Direct observation of oscillatory behaviour suggesting two closely equivalent ubiquinones. Biochim Biophys Acta 459:525–531
Acknowledgments
The work was supported by a grant from the Italian Ministry of Education Prin MIUR 2010 (2010C4R8M8). Donato Frascati and Annalisa Bottalico's help with some experimental measurements is acknowledged. We thank the members of the European Cooperation in Science and Technology network, PHOTOTECH COST TD1102, for helpful discussions.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ciriaco, F., Tangorra, R.R., Antonucci, A. et al. Semiquinone oscillations as a tool for investigating the ubiquinone binding to photosynthetic reaction centers. Eur Biophys J 44, 183–192 (2015). https://doi.org/10.1007/s00249-015-1013-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00249-015-1013-1