Abstract
Photosystem I from the menB strain of Synechocystis sp. PCC 6803 containing foreign quinones in the A1 sites was used for studying the primary steps of electron transfer by pump-probe femtosecond laser spectroscopy. The free energy gap (− ΔG) of electron transfer between the reduced primary acceptor A0 and the quinones bound in the A1 site varied from 0.12 eV for the low-potential 1,2-diamino-anthraquinone to 0.88 eV for the high-potential 2,3-dichloro-1,4-naphthoquinone, compared to 0.5 eV for the native phylloquinone. It was shown that the kinetics of charge separation between the special pair chlorophyll P700 and the primary acceptor A0 was not affected by quinone substitutions, whereas the rate of A0 → A1 electron transfer was sensitive to the redox-potential of quinones: the decrease of − ΔG by 400 meV compared to the native phylloquinone resulted in a ~ fivefold slowing of the reaction The presence of the asymmetric inverted region in the ΔG dependence of the reaction rate indicates that the electron transfer in photosystem I is controlled by nuclear tunneling and should be treated in terms of quantum electron–phonon interactions. A three-mode implementation of the multiphonon model, which includes modes around 240 cm−1 (large-scale protein vibrations), 930 cm−1 (out-of-plane bending of macrocycles and protein backbone vibrations), and 1600 cm−1 (double bonds vibrations) was applied to rationalize the observed dependence. The modes with a frequency of at least 1600 cm−1 make the predominant contribution to the reorganization energy, while the contribution of the “classical” low-frequency modes is only 4%.
Similar content being viewed by others
Data availability
Data are available upon request by the corresponding authors.
Abbreviations
- PS:
-
Photosystem
- ΔG:
-
Free energy difference
- P700 :
-
Chlorophyll dimer—primary electron donor
- A0 :
-
Primary chlorophyll acceptor
- A1 :
-
Secondary quinone acceptor
- Chl:
-
Chlorophyll
- RC:
-
Reaction center
- bRC:
-
Bacterial reaction center
- ET:
-
Electron transfer
- SHE:
-
The standard hydrogen electrode
- SCE:
-
The saturated calomel electrode
- PhQ:
-
Phylloquionone
- PQ:
-
Plastoquinone
- DCNQ:
-
2,3-Dichloro-1,4-naphthoquinone
- NQ18:
-
2-Octadecyl-amino-1,4-naphthoquinone
- AQ:
-
Anthraquinone
- 1-AQ:
-
1-Aminoanthraquinone
- 2-AQ:
-
2-Aminoanthraquinone
- 1,2-AQ:
-
1,2-Diaminoanthraquinone
- 1,5-AQ:
-
1,5-Diaminoanthraquinone
References
Akhtar P, Caspy I, Nowakowski PJ et al (2021) Two-dimensional electronic spectroscopy of a minimal photosystem I complex reveals the rate of primary charge separation. J Am Chem Soc 143:14601–14612. https://doi.org/10.1021/jacs.1c05010
Bevington PR, Robinson DK (1992) Data reduction and error analysis for the physical sciences. McGraw-Hill Inc, New York
Bixon M, Jortner J (1986) Coupling of protein modes to electron transfer in bacterial photosynthesis. J Phys Chem 90:3795–3800. https://doi.org/10.1021/j100407a055
Bixon M, Jortner J (1989) Activationless and pseudoactivationless primary electron transfer in photosynthetic bacterial reaction centers. Chem Phys Lett 159:17–20. https://doi.org/10.1016/S0009-2614(89)87445-7
Bixon M, Jortner J (1991) Non-Arrhenius temperature dependence of electron-transfer rates. J Phys Chem 95:1941–1944. https://doi.org/10.1021/j100158a011
Bixon M, Jortner J, Michel-Beyerle ME (1995) A kinetic analysis of the primary charge separation in bacterial photosynthesis. Energy gaps and static heterogeneity. Chem Phys 197:389–404. https://doi.org/10.1016/0301-0104(95)00168-N
Borrelli R, Di Donato M, Peluso A (2007a) Quantum dynamics of electron transfer from bacteriochlorophyll to pheophytin in bacterial reaction centers. J Chem Theory Comput 3:673–680. https://doi.org/10.1021/ct6003802
Borrelli R, Di Donato M, Peluso A (2007b) Electron transfer rates and Franck–Condon factors: an application to the early electron transfer steps in photosynthetic reaction centers. Theor Chem Acc 117:957–967. https://doi.org/10.1007/s00214-006-0215-0
Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta Bioenerg 1318:322–373. https://doi.org/10.1016/S0005-2728(96)00112-0
Brettel K, Leibl W (2001) Electron transfer in photosystem I. Biochim Biophys Acta Bioenerg 1507:100–114. https://doi.org/10.1016/S0005-2728(01)00202-X
Brettel K, Vos MH (1999) Spectroscopic resolution of the picosecond reduction kinetics of the secondary electron acceptor A1 in photosystem I. FEBS Lett 447:315–317. https://doi.org/10.1016/S0014-5793(99)00317-8
Brodsky AE, Gordienko LL, Degtiarev LS (1968) Cathodic reduction of some aromatic compounds to free anion-radicals. Electrochim Acta 13:1095–1100. https://doi.org/10.1016/0013-4686(68)80038-6
Cherepanov DA, Drevenstedt W, Krishtalik LI et al (1998) Protein relaxation and kinetics of P 680 + reduction in photosystem II. In: Cherepanov DA et al (eds) Photosynthesis: mechanisms and effects. Springer, Dordrecht, pp 1073–1076
Cherepanov DA, Krishtalik LI, Mulkidjanian AY (2001) Photosynthetic electron transfer controlled by protein relaxation: analysis by Langevin stochastic approach. Biophys J 80:1033–1049. https://doi.org/10.1016/S0006-3495(01)76084-5
Cherepanov DA, Milanovsky GE, Petrova AA et al (2017a) Electron transfer through the acceptor side of photosystem I: interaction with exogenous acceptors and molecular oxygen. Biochem Mosc 82:1249–1268. https://doi.org/10.1134/S0006297917110037
Cherepanov DA, Shelaev IV, Gostev FE et al (2017b) Mechanism of adiabatic primary electron transfer in photosystem I: femtosecond spectroscopy upon excitation of reaction center in the far-red edge of the Q Y band. Biochim Biophys Acta Bioenerg 1858:895–905. https://doi.org/10.1016/j.bbabio.2017.08.008
Cherepanov DA, Milanovsky GE, Gopta OA et al (2018) Electron–phonon coupling in cyanobacterial photosystem I. J Phys Chem B 122:7943–7955. https://doi.org/10.1021/acs.jpcb.8b03906
Cherepanov DA, Shelaev IV, Gostev FE et al (2020a) Generation of ion-radical chlorophyll states in the light-harvesting antenna and the reaction center of cyanobacterial photosystem I. Photosynth Res. https://doi.org/10.1007/s11120-020-00731-0
Cherepanov DA, Shelaev IV, Gostev FE et al (2020b) Evidence that chlorophyll f functions solely as an antenna pigment in far-red-light photosystem I from Fischerella thermalis PCC 7521. Biochim Biophys Acta Bioenerg 1861:148184. https://doi.org/10.1016/j.bbabio.2020.148184
Cherepanov DA, Shelaev IV, Gostev FE et al (2021a) Primary charge separation within the structurally symmetric tetrameric Chl2APAPBChl2B chlorophyll exciplex in photosystem I. J Photochem Photobiol B Biol 217:112154. https://doi.org/10.1016/j.jphotobiol.2021.112154
Cherepanov DA, Shelaev IV, Gostev FE et al (2021b) Symmetry breaking in photosystem I: ultrafast optical studies of variants near the accessory chlorophylls in the A- and B-branches of electron transfer cofactors. Photochem Photobiol Sci 20:1209–1227. https://doi.org/10.1007/s43630-021-00094-y
Cherepanov DA, Petrova AA, Mamedov MD et al (2022a) Comparative absorption dynamics of the singlet excited states of Chlorophylls a and d. Biochem Mosc 87:1179–1186. https://doi.org/10.1134/S000629792210011X
Cherepanov DA, Semenov AY, Mamedov MD et al (2022b) Current state of the primary charge separation mechanism in photosystem I of cyanobacteria. Biophys Rev 14:805–820. https://doi.org/10.1007/s12551-022-00983-1
Chirico S, Drago E, Golbeck JH, et al (2008) Transient EPR studies of in vivo uptake of substituted anthraquinones by photosystem I in phylloquinone biosynthetic pathway mutants of Synechocystis sp. PCC 6803. In: Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 227–230
Closs GL, Miller JR (1988) Intramolecular long-distance electron transfer in organic molecules. Science 240:440–447. https://doi.org/10.1126/science.240.4851.440
Coates CS, Ziegler J, Manz K et al (2013) The structure and function of quinones in biological solar energy transduction: a cyclic voltammetry, epr, and hyperfine sub-level correlation (HYSCORE) spectroscopy study of model naphthoquinones. J Phys Chem B 117:7210–7220. https://doi.org/10.1021/jp401024p
Dobryakov AL, Pérez Lustres JL, Kovalenko SA, Ernsting NP (2008) Femtosecond transient absorption with chirped pump and supercontinuum probe: perturbative calculation of transient spectra with general lineshape functions, and simplifications. Chem Phys 347:127–138. https://doi.org/10.1016/j.chemphys.2007.11.003
Fleming GR, Cho M (1996) Chromophore-solvent dynamics. Annu Rev Phys Chem 47:109–134. https://doi.org/10.1146/annurev.physchem.47.1.109
Fromme P, Jordan P, Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta Bioenerg 1507:5–31. https://doi.org/10.1016/S0005-2728(01)00195-5
Fukuzumi S, Ohkubo K, Imahori H, Guldi DM (2003) Driving force dependence of intermolecular electron-transfer reactions of fullerenes. Chem A Eur J 9:1585–1593. https://doi.org/10.1002/chem.200390182
Giera W, Gibasiewicz K, Ramesh VM et al (2009) Electron transfer from A0̄ to A1 in photosystem I from Chlamydomonas reinhardtii occurs in both the A and B branch with 25–30-ps lifetime. Phys Chem Chem Phys 11:5186–5191. https://doi.org/10.1039/b822938d
Giera W, Ramesh VM, Webber AN et al (2010) Effect of the P700 pre-oxidation and point mutations near A0 on the reversibility of the primary charge separation in photosystem I from Chlamydomonas reinhardtii. Biochim Biophys Acta Bioenerg 1797:106–112. https://doi.org/10.1016/j.bbabio.2009.09.006
Golbeck JH, Parrett KG, McDermott AE (1987) Photosystem I charge separation in the absence of center A and B. III. Biochemical characterization of a reaction center particle containing P-700 and FX. Biochem Bioiphys Acta Bioenerg 893:149–160. https://doi.org/10.1016/0005-2728(87)90034-X
Golubeva EN, Zubanova EM, Melnikov MY et al (2014) Femtosecond spectroscopy and TD-DFT calculations of CuCl 4 2− excited states. Dalt Trans 43:17820–17827. https://doi.org/10.1039/C4DT01409J
Gorka M, Cherepanov DA, Semenov AY, Golbeck JH (2020) Control of electron transfer by protein dynamics in photosynthetic reaction centers. Crit Rev Biochem Mol Biol 55:425–468. https://doi.org/10.1080/10409238.2020.1810623
Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723. https://doi.org/10.1002/elps.1150181505
Gunner MR, Dutton PL (1989) Temperature and −ΔG° dependence of the electron transfer from BPh- to QA in reaction center protein from Rhodobacter sphaeroides with different quinones as QA. J Am Chem Soc 111:3400–3412. https://doi.org/10.1021/ja00191a043
Gunner MR, Robertson DE, Dutton PL (1986) Kinetic studies on the reaction center protein from Rhodopseudomonas sphaeroides: the temperature and free energy dependence of electron transfer between various quinones in the QA site and the oxidized bacteriochlorophyll dimer. J Phys Chem 90:3783–3795. https://doi.org/10.1021/j100407a054
Herascu N, Hunter MS, Shafiei G et al (2016) Spectral hole burning in cyanobacterial photosystem I with P700 in oxidized and neutral states. J Phys Chem B 120:10483–10495. https://doi.org/10.1021/acs.jpcb.6b07803
Holzwarth AR, Müller MG, Niklas J, Lubitz W (2005) Charge recombination fluorescence in photosystem I reaction centers from Chlamydomonas reinhardtii. J Phys Chem B 109:5903–5911. https://doi.org/10.1021/jp046299f
Hopfield JJ (1974) Electron transfer between biological molecules by thermally activated tunneling. Proc Natl Acad Sci 71:3640–3644. https://doi.org/10.1073/pnas.71.9.3640
Itoh S, Iwaki M, Ikegami I (2001) Modification of photosystem I reaction center by the extraction and exchange of chlorophylls and quinones. Biochim Biophys Acta Bioenerg 1507:115–138. https://doi.org/10.1016/S0005-2728(01)00199-2
Iwaki M, Itoh S (1994) Reaction of reconstituted acceptor quinone and dynamic equilibration of electron-transfer in the photosystem-I reaction-center. Plant Cell Physiol 35:983–993
Iwaki M, Kumazaki S, Yoshihara K et al (1996) ΔG0 dependence of the electron transfer rate in the photosynthetic reaction center of plant photosystem I: natural optimization of reaction between chlorophyll a (A0) and quinone. J Phys Chem 100:10802–10809. https://doi.org/10.1021/jp960221k
Johnson TW, Shen G, Zybailov B et al (2000) Recruitment of a foreign quinone into the A1 site of photosystem I. I. Genetic and physiological characterization of phylloquinone biosynthetic pathway mutants in Synechocystis sp. PCC 6803. J Biol Chem 275:8523–8530. https://doi.org/10.1074/jbc.275.12.8523
Johnson TW, Zybailov B, Jones AD et al (2001) Recruitment of a foreign quinone into the A1 site of photosystem I: in vivo replacement of plastoquinone-9 by media-supplemented naphthoquinones in phylloquinone biosynthetic pathway mutants of Synechocystis sp. PCC 6803. J Biol Chem 276:39512–39521. https://doi.org/10.1074/jbc.M104040200
Jones R, Spotswood TM (1962) Polarography of anthraquinone derivatives in dimethylformamide: effect of hydrogen bonding. Aust J Chem 15:492–502. https://doi.org/10.1071/Ch9620492
Jordan P, Fromme P, Witt HT et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. https://doi.org/10.1038/35082000
Jortner J (1976) Temperature dependent activation energy for electron transfer between biological molecules. J Chem Phys 64:4860–4867. https://doi.org/10.1063/1.432142
Jumper CC, Arpin PC, Turner DB et al (2016) Broad-band pump-probe spectroscopy quantifies ultrafast solvation dynamics of proteins and molecules. J Phys Chem Lett 7:4722–4731. https://doi.org/10.1021/acs.jpclett.6b02237
Kato Y, Noguchi T (2022) Redox properties and regulatory mechanism of the iron-quinone electron acceptor in photosystem II as revealed by FTIR spectroelectrochemistry. Photosynth Res 152:135–151. https://doi.org/10.1007/s11120-021-00894-4
Kleinherenbrink FAM, Hastings G, Blankenship RE, Wittmershaus BP (1994) Delayed fluorescence from Fe-S type photosynthetic reaction centers at low redox potential. Biochemistry 33:3096–3105. https://doi.org/10.1021/bi00176a044
Kumazaki S, Iwaki M, Ikegami I et al (1994) Rates of primary electron transfer reactions in the photosystem I reaction center reconstituted with different quinones as the secondary acceptor. J Phys Chem 98:11220–11225. https://doi.org/10.1021/j100094a033
LeBard DN, Kapko V, Matyushov DV (2008) Energetics and kinetics of primary charge separation in bacterial photosynthesis. J Phys Chem B 112:10322–10342. https://doi.org/10.1021/jp8016503
Lee EJ, Medvedev ES, Stuchebrukhov AA (2000) Effect of quantum modes in biological electron transfer reactions: a useful approximation for the harmonic model with frequency change and Duchinsky rotation. J Chem Phys 112:9015–9024. https://doi.org/10.1063/1.481513
Leggett AJ, Chakravarty S, Dorsey AT et al (1987) Dynamics of the dissipative two-state system. Rev Mod Phys 59:1–85. https://doi.org/10.1103/RevModPhys.59.1
Levich VG, Dogonadze RR (1959) Theory of non-radiation electron transitions from ion to ion in solutions. Dokl Akad Nauk SSSR 124:123–126
Li Y, Van Der Est A, Lucas MG et al (2006) Directing electron transfer within photosystem I by breaking H-bonds in the cofactor branches. Proc Natl Acad Sci USA 103:2144–2149. https://doi.org/10.1073/pnas.0506537103
Lin X, Murchison HA, Nagarajan V et al (1994) Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 91:10265–10269. https://doi.org/10.1073/pnas.91.22.10265
Makita H, Hastings G (2016) Modeling electron transfer in photosystem I. Biochim Biophys Acta Bioenerg 1857:723–733. https://doi.org/10.1016/j.bbabio.2016.03.015
Makita H, Hastings G (2017) Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency. Proc Natl Acad Sci USA 114:9267–9272. https://doi.org/10.1073/pnas.1704855114
Marchi M, Gehlen JN, Chandler D, Newton M (1993) Diabatic surfaces and the pathway for primary electron transfer in a photosynthetic reaction center. J Am Chem Soc 115:4178–4190. https://doi.org/10.1021/ja00063a041
Marcus RA (1956) On the Theory of oxidation-reduction reactions involving electron transfer. I J Chem Phys 24:966–978. https://doi.org/10.1063/1.1742723
McMahon BH, Müller JD, Wraight CA, Nienhaus GU (1998) Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys J 74:2567–2587. https://doi.org/10.1016/S0006-3495(98)77964-0
Melkozernov AN, Lin S, Blankenship RE (2000) Excitation dynamics and heterogeneity of energy equilibration in the core antenna of photosystem I from the Cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 39:1489–1498. https://doi.org/10.1021/bi991644q
Milanovsky GE, Petrova AA, Cherepanov DA, Semenov AY (2017) Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors. Photosynth Res 133:185–199. https://doi.org/10.1007/s11120-017-0366-y
Molotokaite E, Remelli W, Casazza AP et al (2017) Trapping dynamics in photosystem I-light harvesting complex I of higher plants is governed by the competition between excited state diffusion from low energy states and photochemical charge separation. J Phys Chem B 121:9816–9830. https://doi.org/10.1021/acs.jpcb.7b07064
Mula S, Savitsky A, Möbius K et al (2012) Incorporation of a high potential quinone reveals that electron transfer in photosystem I becomes highly asymmetric at low temperature. Photochem Photobiol Sci 11:946–956. https://doi.org/10.1039/c2pp05340c
Okamura MY, Isaacson RA, Feher G (1975) Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc Natl Acad Sci USA 72:3491–3495. https://doi.org/10.1073/pnas.72.9.3491
Parrett KG, Mehari T, Warren PG, Golbeck JH (1989) Purification and properties of the intact P-700 and Fx-containing photosystem I core protein. Biochim Biophys Acta 973:324–332. https://doi.org/10.1016/S0005-2728(89)80439-6
Parson WW (2018) Electron-transfer dynamics in a zn-porphyrin-quinone cyclophane: effects of solvent, vibrational relaxations, and conical intersections. J Phys Chem B. https://doi.org/10.1021/acs.jpcb.8b01072
Parson WW, Warshel A (2004) A density-matrix model of photosynthetic electron transfer with microscopically estimated vibrational relaxation times. Chem Phys 296:201–216. https://doi.org/10.1016/j.chemphys.2003.10.006
Patil R, Bhand S, Konkimalla VB et al (2016) Molecular association of 2-(n-alkylamino)-1,4-naphthoquinone derivatives: electrochemical, DFT studies and antiproliferative activity against leukemia cell lines. J Mol Struct 1125:272–281. https://doi.org/10.1016/j.molstruc.2016.06.075
Peloquin JM, Williams JC, Lin X et al (1994) Time-dependent thermodynamics during early electron transfer in reaction centers from Rhodobacter sphaeroides. Biochemistry 33:8089–8100
Petrova AA, Boskhomdzhieva BKBK, Milanovsky GEGE et al (2017) Interaction of various types of photosystem I complexes with exogenous electron acceptors. Photosynth Res 133:175–184. https://doi.org/10.1007/s11120-017-0371-1
Popescu SD, Barbacaru E (1985) A polarographic study of some aminoanthraquinones. Anal Lett 18:947–956. https://doi.org/10.1080/00032718508066190
Prince RC, Leslie Dutton P, Malcolm Bruce J (1983) Electrochemistry of ubiquinones. Menaquinones and plastoquinones in aprotic solvents. FEBS Lett 160:273–276. https://doi.org/10.1016/0014-5793(83)80981-8
Prince RC, Dutton PL, Gunner MR (2022) The aprotic electrochemistry of quinones. Biochim Biophys Acta Bioenerg 1863:148558. https://doi.org/10.1016/j.bbabio.2022.148558
Ptushenko VV, Cherepanov DA, Krishtalik LI, Semenov AY (2008) Semi-continuum electrostatic calculations of redox potentials in photosystem I. Photosynth Res 97:55–74. https://doi.org/10.1007/s11120-008-9309-y
Pushkar YN, Zech SG, Stehlik D et al (2002) Orientation and protein-cofactor interactions of monosubstituted n-alkyl naphthoquinones in the A1 binding site of photosystem I. J Phys Chem B 106:12052–12058. https://doi.org/10.1021/jp0265743
Pushkar YN, Golbeck JH, Stehlik D, Zimmermann H (2004) Asymmetric hydrogen-bonding of the quinone cofactor in photosystem I probed by 13C-labeled naphthoquinones. J Phys Chem B 108:9439–9448. https://doi.org/10.1021/jp0361879
Pushkar YN, Karyagina I, Stehlik D et al (2005) Recruitment of a foreign quinone into the A1 site of photosystem I: consecutive forward electron transfer from A0 to A1 to FX with anthraquinone in the A1 site as studied by transient EPR. J Biol Chem 280:12382–12390. https://doi.org/10.1074/jbc.M412940200
Rätsep M, Johnson TW, Chitnis PR, Small GJ (2000) The red-absorbing chlorophyll a antenna states of photosystem I: a hole-burning Study of Synechocystis sp. PCC 6803 and its mutants. J Phys Chem B 104:836–847. https://doi.org/10.1021/jp9929418
Sakuragi Y, Zybailov B, Shen G et al (2005) Recruitment of a foreign quinone into the A1 site of photosystem I: characterization of a menB rubA double deletion mutant in Synechococcus sp. PCC 7002 devoid of FX, FA, and FB and containing plastoquinone or exchanged 9,10-anthraquinone. J Biol Chem 280:12371–12381. https://doi.org/10.1074/jbc.M412943200
Santabarbara S, Heathcote P, Evans MCW (2005) Modelling of the electron transfer reactions in photosystem I by electron tunnelling theory: the phylloquinones bound to the PsaA and the PsaB reaction centre subunits of PS I are almost isoenergetic to the iron-sulfur cluster FX. Biochim Biophys Acta Bioenerg 1708:283–310. https://doi.org/10.1016/j.bbabio.2005.05.001
Savikhin S, Xu W, Chitnis PR, Struve WS (2000) Ultrafast primary processes in PS I from Synechocystis sp. PCC 6803: roles of P700 and A0. Biophys J 79:1573–1586. https://doi.org/10.1016/S0006-3495(00)76408-3
Savikhin S, Xu W, Martinsson P et al (2001) Kinetics of charge separation and A0− → A1 electron transfer in photosystem I reaction centers. Biochemistry 40:9282–9290. https://doi.org/10.1021/bi0104165
Schenderlein M, Çetin M, Barber J et al (2008) Spectroscopic studies of the chlorophyll d containing photosystem I from the cyanobacterium, Acaryochloris marina. Biochim Biophys Acta Bioenerg 1777:1400–1408. https://doi.org/10.1016/j.bbabio.2008.08.008
Schmidt MW, Baldridge KK, Boatz JA et al (1993) General atomic and molecular electronic structure system. J Comput Chem 14:1347–1363. https://doi.org/10.1002/jcc.540141112
Schulten K, Tesch M (1991) Coupling of protein motion to electron transfer: Molecular dynamics and stochastic quantum mechanics study of photosynthetic reaction centers. Chem Phys 158:421–446. https://doi.org/10.1016/0301-0104(91)87081-6
Schuster DI, Cheng P, Jarowski PD et al (2004) Design, synthesis, and photophysical studies of a porphyrin-fullerene dyad with parachute topology; charge recombination in the marcus inverted region. J Am Chem Soc 126:7257–7270. https://doi.org/10.1021/ja038676s
Semenov AY, Vassiliev IR, van Der Est A et al (2000) Recruitment of a foreign quinone into the A1 site of photosystem I. Altered kinetics of electron transfer in phylloquinone biosynthetic pathway mutants studied by time-resolved optical, EPR, and electrometric techniques. J Biol Chem 275:23429–23438. https://doi.org/10.1074/jbc.M000508200
Shelaev IV, Gostev FE, Mamedov MD et al (2010) Femtosecond primary charge separation in Synechocystis sp. PCC 6803 photosystem I. Biochim Biophys Acta Bioenerg 1797:1410–1420. https://doi.org/10.1016/j.bbabio.2010.02.026
Shuvalov VA (1976) The study of the primary photoprocesses in photosystem I of chloroplasts recombination luminescence, chlorophyll triplet state and triplet-triplet annihilation. Biochim Biophys Acta Bioenerg 430:113–121. https://doi.org/10.1016/0005-2728(76)90227-9
Singh UC, Kollman PA (1984) An approach to computing electrostatic charges for molecules. J Comput Chem 5:129–145. https://doi.org/10.1002/jcc.540050204
Souaille M, Marchi M (1997) Nuclear dynamics and electronic transition in a photosynthetic reaction center. J Am Chem Soc 119:3948–3958. https://doi.org/10.1021/ja943841c
Srinivasan N, Golbeck JH (2009) Protein-cofactor interactions in bioenergetic complexes: the role of the A1A and A1B phylloquinones in Photosystem I. Biochim Biophys Acta 1787:1057–1088. https://doi.org/10.1016/j.bbabio.2009.04.010
Van Der Est A (2001) Light-induced spin polarization in type I photosynthetic reaction centres. Biochim Biophys Acta Bioenerg 1507:212–225. https://doi.org/10.1016/S0005-2728(01)00204-3
Vos MH, van Gorkom HJ (1990) Thermodynamical and structural information on photosynthetic systems obtained from electroluminescence kinetics. Biophys J 58:1547–1555. https://doi.org/10.1016/S0006-3495(90)82499-1
Wang H, Lin S, Katilius E et al (2009) Unusual temperature dependence of photosynthetic electron transfer due to protein dynamics. J Phys Chem B 113:818–824. https://doi.org/10.1021/jp807468c
Warshel A, Parson WW (1991) Computer simulations of electron-transfer reactions in solution and in photosynthetic reaction centers. Annu Rev Phys Chem 42:279–309. https://doi.org/10.1146/annurev.pc.42.100191.001431
Woodbury NW, Parson WW (1986) Nanosecond fluorescence from chromatophores of Rhodopseudomonas sphaeroides and Rhodospirillum rubrum. Biochim Biophys Acta Bioenerg 850:197–210. https://doi.org/10.1016/0005-2728(86)90174-X
Acknowledgements
This article is dedicated to the memory of the outstanding biophysicist Vladimir Shuvalov, with whom most authors had the honor to work closely over the past 15 years of his life. This work was supported by Lomonosov Moscow State University Program of Development. Optical measurements were performed using core research facilities of FRCCP RAS (No. 1440743, 506694).
Funding
This work was supported by the Russian Science Foundation Grant RSF 22-24-00705.
Author information
Authors and Affiliations
Contributions
A.S., W.J. and V.N. developed the concept and methodology of experiments. W.J. carried out the substitution of quinones, the isolation of PS I preparations, EPR, Cyclic Voltammetry and HPLC measurements. I.S., F.G. and M.M. performed femtosecond measurements and data collections. A.A. carried out analysis of the spectroscopy data. D.C. analyzed electrochemical data, developed the multiphonon model, and wrote the first draft of the manuscript. All authors reviewed the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cherepanov, D., Aybush, A., Johnson, T.W. et al. Inverted region in the reaction of the quinone reduction in the A1-site of photosystem I from cyanobacteria. Photosynth Res 159, 115–131 (2024). https://doi.org/10.1007/s11120-023-01020-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-023-01020-2