Abstract
Light excitation of chlorophylls and bacteriochlorophylls creates strong reductants to initiate guided electron transfer through chains of redox centers, converting light energy into electrostatic and chemical redox energy and largely avoiding the threat of charge recombination unless useful. Most electron-transfer reactions of photosynthesis are single-electron transfers between well-separated redox centers via electron tunneling through the insulating intervening protein medium. Tunneling rates are dominated by an exponential dependence on the edge-to-edge distance between cofactors. There is an approximately Gaussian dependence of rate on driving force, with a peak rate at the reorganization energy, as defined by classical Marcus theory and modified to include quantum effects. Complex quantum theoretical rate dependencies are well approximated by a simple empirical expression with three parameters: distance, driving force, and reorganization energy. Natural selection exploits distance and driving force to speed desirable electron transfers or slow undesirable electron transfer. Redox centers engaged in productive electron transfer are placed less than 14 Å apart. Natural photosynthetic proteins are far from ideal: they have high yields but a superabundance of cofactors and relatively large energy losses.
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Abbreviations
- ADP:
-
Adenosine diphosphate
- ATP:
-
Adenosine triphosphate
- NADH:
-
Reduced nicotinamide adenine dinucleotide
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- λ:
-
Reorganization energy
- ΔG:
-
Free energy of reaction
- ℏω:
-
Characteristic frequency of vibration coupled to electron transfer
References
Byrdin M, Lukacs A, Thiagarajan V, Eker APM, Brettel K, Vos MH. Quantum yield measurements of short-lived photoactivation intermediates in DNA photolyase: toward a detailed understanding of the triple tryptophan electron transfer chain. J Phys Chem A. 2010;114(9):3207–14.
Zeugner A, Byrdin M, Bouly JP, Bakrim N, Giovani B, Brettel K, et al. Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. J Biol Chem. 2005;280(20):19437–40.
Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J. Kinetics and pathways of charge recombination in photosystem II. Biochemistry. 2002;41(26):8518–27.
Krabben L, Schlodder E, Jordan R, Carbonera D, Giacometti G, Lee H, et al. Influence of the axial ligands on the spectral properties of P700 of photosystem I: a study of site-directed mutants. Biochemistry. 2000;39(42):13012–25.
Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution. Nature. 2001;411(6840):909–17.
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science. 2004;303(5665):1831–8.
Deisenhofer J, Epp O, Sinning H, Michel H. Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from rhodopseudomonas viridis. J Mol Biol. 1995;246:429–57.
Kee HL, Kirmaier C, Tang Q, Diers JR, Muthiah C, Taniguch M, et al. Effects of substituents on synthetic analogs of chlorophylls. Part 1: synthesis, vibrational properties and excited-state decay characteristics. Photochem Photobiol. 2007;83(5):1110–24.
Rutherford AW, Osyczka A, Rappaport F. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O-2. FEBS Lett. 2012;586(5):603–16.
Gorman AA, Rodgers MAJ. Current perspectives of singlet oxygen detection in biological environments. J Photochem Photobiol B. 1992;14(3):159–76.
Sies H, Menck CFM. Singlet oxygen induced DNA damage. Mutat Res. 1992;275(3–6):367–75.
Trebst A, Depka B, Hollander-Czytko H. A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett. 2002;516(1–3):156–60.
Pross A. The single electron shift as a fundamental process in organic chemistry: the relationship between polar and electron-transfer pathways. Acc Chem Res. 1985;18:212–9.
Eberson L. Electron transfer reactions in organic chemistry. New York: Springer-Verlag; 1987. 234 p.
Devault D. Quantum-mechanical tunnelling in biological-systems. Q Rev Biophys. 1980;13(4):387–564.
Devault D, Chance B. Studies of photosynthesis using a pulsed laser. I Temperature dependence of cytochrome oxidation rate in Chromatium. Evidence for tunneling. Biophys J. 1966;6(6):825–47.
Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL. Nature of biological electron-transfer. Nature. 1992;355(6363):796–802.
Eyring H. The activated complex in chemical reactions. J Chem Phys. 1935;3:107–15.
Zwolinski BJ, Marcus RJ, Eyring H. Inorganic oxidation-reduction reactions in solution-electron transfers. Chem Rev. 1955;55(1):157–80.
Moser CC, Anderson JLR, Dutton PL. Guidelines for tunneling in enzymes. Biochim Biophys Acta. 2010;1797(8):1573–86.
Marcus RA. On the theory of oxidation-reduction reactions involving electron transfer: I. J Chem Phys. 1956;24:966–78.
Gunner MR, Dutton PL. Temperature and -delta-G-degrees 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. 1989;111(9):3400–12.
Iwaki M, Kumazaki S, Yoshihara K, Erabi T, Itoh S. Delta G(0) dependence of the electron transfer rate in the photosynthetic reaction center of plant photosystem I: Natural optimization of reaction between chlorophyll a (A(0)) and quinone. J Phys Chem. 1996;100(25):10802–9.
Lin X, Williams JC, Allen JP, Mathis P. Relationship between rate and free-energy difference for electron-transfer from cytochrome C(2) to the reaction-center in rhodobacter-sphaeroides. Biochemistry. 1994;33(46):13517–23.
Woodbury NW, Parson WW, Gunner MR, Prince RC, Dutton PL. Radical-pair energetics and decay mechanisms in reaction centers containing anthraquinones, naphthoquinones or benzoquinones in place of ubiquinone. Biochim Biophys Acta. 1986;851(1):6–22.
Lin X, Murchison HA, Nagarajan V, Parson WW, Allen JP, Williams JC. Specific alteration of the oxidation potential of the electron-donor in reaction centers from rhodobacter-sphaeroides. Proc Natl Acad Sci U S A. 1994;91(22):10265–9.
Hopfield JJ. Electron transfer between biological molecules by thermally activated tunneling. Proc Natl Acad Sci U S A. 1974;71:3640–4.
Jortner J. Temperature-dependent activation-energy for electron-transfer between biological molecules. J Chem Phys. 1976;64(12):4860–7.
Crofts AR, Rose S. Marcus treatment of endergonic reactions: a commentary. Biochim Biophy Acta. 2007;1767(10):1228–32.
Moser CC, Chobot SE, Page CC, Dutton PL. Distance metrics for heme protein electron tunneling. Biochim Biophy Acta. 2008;1777(7–8):1032–7.
Page CC, Moser CC, Chen XX, Dutton PL. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature. 1999;402(6757):47–52.
Evans MCW, Heathcote P. Effects of glycerol on the redox properties of the electron-acceptor complex in spinach photosystem-I particles. Biochim Biophy Acta. 1980;590(1):89–96.
Acknowledgments
This didactic account is the result of the development of engineering for man-made oxidoreductases of the kind proposed in Office of Basic Energy Sciences, Division of Materials Sciences and Engineering [DE-FG02-05ER46223], and the US National Institutes of Health, General Medical Institutes [RO1 GM 41048]. The support from each is nearly equal.
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Moser, C.C. (2014). Tunneling in Electron Transport. In: Golbeck, J., van der Est, A. (eds) The Biophysics of Photosynthesis. Biophysics for the Life Sciences, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1148-6_4
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DOI: https://doi.org/10.1007/978-1-4939-1148-6_4
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