Abstract
Photosynthetic reaction center (RC) pigment protein complex converts the free energy of light into chemical potential of charge pairs with extremely high efficiency. A transient phase in the absorption spectrum in the sub-millisecond time scale is expected to be especially important to examine the conformational gating model of the Q −A QB to QAQ −B (here QA and QB are the primary and secondary quinone type electron acceptors, respectively) electron transport. Essential kinetic components at few tens of microseconds scale and at around 200 μs have been suggested. We investigated the conformation change of RCs using heterodyne detection of the laser-induced transient grating method. An about 25 μs dynamics was observed, which coincides with the one described by the conformational gating model and possibly related to the nonadiabatic intrinsic Q −A QB to QAQ −B electron transport. The relative intensity of this component decreased with increasing quinone concentration indicating an initial (P+Q −A )1 or a relaxed (P+Q −A )2 conformational substate. We did not find the decay component at few hundreds of microseconds time scale indicating that there is no large displacement in the RC structure if QB is present. The diffusion coefficient of the RC/LDAO detergent micelles calculated from the kinetic component was D = 3.8 × 10−11 m2/s that agrees fairly well with the number estimated from the Einstein–Stokes relationship, and relates to a hydrodynamic diameter of 11.4 nm of the RC in LDAO micellar solution.
Similar content being viewed by others
References
Alexov EG, Gunner MR (1999) Calculated protein and proton motions coupled to electron transfer: electron transfer from Q −A to QB in bacterial photosynthetic reaction centers. Biochemistry 38:8253–8270
Allen JP, Williams JC (1998) Photosynthetic reaction centers. FEBS Lett 438:5–9
Angerhofer A, Bornhäuser F, Aust V, Hartwich G, Scheer H (1998) Triplet energy transfer in bacterial photosynthetic reaction centres. Biochim Biophys Acta 1365:404–420
Arata H, Parson WW (1981) Enthalpy and volume changes accompanying electron transfer from P-870 to quinones in Rps. sphaeroides reaction centers. Biochim Biophys Acta 636:70–81
Arellano JB, Yousef YA, Melo TB, Mohamad SBB, Cogdell RJ, Naqvi KR (2007) Formation and geminate quenching of singlet oxygen in purple bacterial reaction center. J Photochem Photobiol B Biol 87:105–112
Baden N, Terazima M (2004) A novel method for measurement of diffusion coefficients of proteins and DNA in solution. Chem Phys Lett 393:539–545
Baxter RHG, Ponomarenko N, Sÿrajer V, Pahl R, Moffat K, Norris JR (2004) Time-resolved crystallographic studies of light-induced structural changes in the photosynthetic reaction center. Proc Natl Acad Sci USA 101:5982–5987
Breton J (2004) Absence of large-scale displacement of quinone QB in bacterial photosynthetic reaction centers. Biochemistry 43:3318–3326
Breton J (2007) Steady state FTIR spectra of the photoreduction of QA and QB in Rhodobacter sphaeroides reaction centers provide evidence against the presence of a proposed transient electron acceptor X between the two quinines. Biochemistry 46:4459–4465
Cherepanov DA, Krishtalik LI, Mulkidjanian AY (2001) Photosynthetic electron transfer controlled by the protein relaxation: analysis by Langevin stochastic approach. Biophys J 80:1033–1049
Dorogi M, Bálint Z, Mikó C, Vileno B, Milas M, Hernádi K, Forró L, Váró Gy, Nagy L (2006) Stabilization effect of single-walled carbon nanotubes on the functioning of photosynthetic reaction centers. J Phys Chem B 110:21473–21479
Edens GJ, Gunner MR, Xu Q, Mauzerall DC (2000) The enthalpy and entropy of reaction for formation of P+Q −A from excited reaction centers of Rhodobacter sphaeroides. J Am Chem Soc 122:1479–1485
Eitoku T, Zarate X, Kozhukh GV, Kim JI, Song PS, Terazima M (2006) Time-resolved detection of conformational changes in oat phytochrome A: time-dependent diffusion. Biophys J 91:3797–3804
Fritzsch G, Koepke J, Diem R, Kuglstatter A, Baciou L (2002) Charge separation induces conformational changes in the photosynthetic reaction centre of purple bacteria. Acta Crystallogr D Biol Crystallogr 58:1660–1663
Goodno GD, Dadusc G, Miller RJD (1998) Ultrafast heterodyne-detected transient-grating spectroscopy using diffractive optics. J Opt Soc Am B 15:1791–1794
Grafton AK, Wheeler RA (1999) Amino acid protonation states determine binding sites of the secondary ubiquinone and its anion in the Rhodobacter sphaeroides photosynthetic reaction center. J Phys Chem B 103:5380–5387
Graige MS, Feher G, Okamura MY (1998) Conformational gating of the electron transfer reaction Q −A QB–QAQ −B in bacterial reaction centers of Rhodobacter sphaeroides determined by driving force assay. Proc Natl Acad Sci USA 95:11679–11684
Hazra P, Inoue K, Laan W, Hellingwerf KJ, Terazima M (2006) Tetramer formation kinetics in the signaling state of AppA monitored by time-resolved diffusion. Biophys J 91:654–661
Hermes S, Stachnik JM, Onidas D, Remy A, Hofman E, Gerwert K (2006) Proton uptake in the reaction center mutant L210DN from Rhodobacter sphaeroides via protonated water molecules. Biochemistry 45:13741–13749
Inoue K, Sasaki J, Morisaki M, Tokunaga F, Terazima M (2004) Time-resolved detection of the sensory rhodopsin II–transducer interaction. Biophys J 87:2587–2597
Khan JS, Imamoto Y, Kataoka M, Tokunaga F, Terazima M (2006) Time-resolved thermodynamics: heat capacity change of transient species during photo-reaction of PYP. J Am Chem Soc 128:1002–1008
Kleinfeld D, Feher G, Okamura MY (1984) Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charged separated state: evidence for light-induced structural changes. Biochemistry 23:5780–5786
Lancaster CRD (1998) Ubiquinone reduction and protonation in photosynthetic reaction centres from Rhodopseudomonas viridis: X-ray structures and their functional implications. Biochim Biophys Acta 1365:143–150
Li J, Gilroy D, Tiede DM, Gunner MR (1998) Kinetic phases in the electron transfer from P+Q −A QB to P+QAQ −B and the associated processes in Rhodobacter sphaeroides R-26 reaction centers. Biochemistry 37:2818–2829
Marchanka A, Paddock M, Lubitz W, Gastel M (2007) Low-temperature pulsed EPR study at 34 GHz of the triplet states of the primary electron donor P865 and the carotenoid in native and mutant bacterial reaction centers of Rhodobacter sphaeroides. Biochemistry 46(51):14782–14794
Mauzerall DC, Gunner MR, Zhang JW (1995) Volume contraction on photoexcitation of the reaction center from Rhodobacter sphaeroides R-26: internal probe of dielectrics. Biophys J 68:275–280
McAuley KE, Fyfe PK, Ridge JP, Cogdell RJ, Isaacs NW, Jones MR (2000) Ubiquinone binding, ubiquinone exclusion, and detailed cofactor conformation in a mutant bacterial reaction center. Biochemistry 39:15032–15043
Nagy L, Kiss V, Brumfeld V, Malkin S (2001) Thermal and structural changes of photosynthetic reaction centers characterized by photoacoustic detection with a broad frequency band hydrophone. Photochem Photobiol 74:81–87
Nagy L, Milano F, Dorogi M, Trotta M, Laczkó G, Szebényi K, Váró Gy, Agostiano A, Maróti P (2004) Protein/lipid interaction in bacterial photosynthetic reaction center: the role of phosphatidylcholine and phosphatidylglycerol in charge stabilization. Biochemistry 43:12913–12923
Nakasone Y, Ono T, Ishii A, Masuda S, Terazima M, (2007) Transient dimerization and conformational change of a BLUF protein: YcgF. J Am Chem Soc 129:7028–7035
Nishihara Y, Sakakura M, Kimura Y, Terazima M (2004) The escape process of carbon monoxide from myoglobin to solution at physiological temperature. J Am Chem Soc 126:11877–11888
Okamura MY, Isaacson RA, Feher G (1975) Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 72:3491–3495
Pokkuluri PR, Laible PD, Deng YL, Wong TN, Hanson DK, Schiffer M (2002) The structure of a mutant photosynthetic reaction center shows unexpected changes in main chain orientations and quinone position. Biochemistry 41:5998–6007
Remy A, Klaus G (2003) Coupling of light-induced electron transfer to proton uptake in photosynthesis. Nat Struct Biol 10:637–644
Rogers JA, Fuchs M, Banet MJ, Hanselman JB, Logan R, Nelson KA (1997) Optical system for rapid materials characterization with the transient grating technique: application to nondestructive evaluation of thin films used in microelectronics. Appl Phys Lett 71:225–227
Sakakura M, Yamaguchi SY, Hirota N, Terazima M (2001) Dynamics of structure and energy of horse carboxymyoglobin after photodissociation of the carbon monoxide. J Am Chem Soc 123:4286–4294
Shuvalov VA, Parson WW (1981) Triplet-states of monomeric bacteriochlorophyll in vitro and of bacteriochlorophyll dimers in antenna and reaction center complexes. Biochim Biophys Acta 638:50–59
Stowell MHB, McPhillips TM, Rees DC, Soltis SM, Abresh E, Feher G (1997) Light induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science 276:812–816
Tandori J, Nagy L, Puskás A, Droppa M, Horváth G, Maróti P (1995) The IleL229 –> Met mutation impairs the quinone binding to the Q −B pocket in reaction centers of Rhodobacter sphaeroides. Photosynth Res 45:135–146
Terazima M (1998) Transient lens spectroscopy in a fast time scale. Isr J Chem 38:143–157
Terazima M (1999a) Optical heterodyne detected transient grating for studies of photochemical reactions and solution dynamics. Chem Phys Lett 304:343–349
Terazima M (1999b) Optical heterodyne detected transient grating for the separation of phase and amplitude gratings. J Phys Chem A 103:7401–7407
Tiede DM, Vazquez J, Cordova J, Marone PA (1996) Time resolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. Biochemistry 35:10763–10775
Turzó K, Laczkó G, Filus Z, Maróti P (2000) Quinone-dependent delayed fluorescence from the reaction center of photosynthetic bacteria. Biophys J 79:14–25
Volk M, Ogrodnik A, Michel-Beyerle M-E (1995) The recombination dynamics of the radical pair P+H− in external magnetic and electric fields. In: Blankensip RE Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 595–626
Walden SE, Wheeler RA (2002) Protein conformational gate controlling binding site preference and migration for ubiquinone-B in the photosynthetic reaction center of Rhodobacter sphaeroides. J Phys Chem B 106:3001–3006
Woodbury NW, Becker M, Middendorf D, Parson WW (1985) Pikosecond kinetics of the initial photochemical electron transfer reaction in bacterial photosynthetic reaction centers. Biochemistry 24:7516–7521
Wraight CA, Clayton R (1974) The absolute quantum efficiency of bacteriochlorophyll photooxidation in reaction centres of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 333:246–260
Zankel KL, Reed DW, Clayton RK (1968) Fluorescence and photochemical quenching in photosynthetic reaction centers. Proc Natl Acad Sci USA 61:1243–1249
Acknowledgments
This work was supported by the grant of Japan Society for Promotion of Science and also by the Grant-in-Aid (nos. 13853002 and 15076204 to M.T.) from the Ministry of Education, Science, Sports, and Culture in Japan.
Author information
Authors and Affiliations
Corresponding author
Additional information
Regional Biophysics Conference of the National Biophysical Societies of Austria, Croatia, Hungary, Italy, Serbia, and Slovenia.
Rights and permissions
About this article
Cite this article
Ohmori, H., Nagy, L., Dorogi, M. et al. Charge stabilization in reaction center protein investigated by optical heterodyne detected transient grating spectroscopy. Eur Biophys J 37, 1167–1174 (2008). https://doi.org/10.1007/s00249-008-0294-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00249-008-0294-z