Abstract
We review the general concept of nonadiabatic quantum spin transitions in biochemistry. A few important examples are highlighted to illustrate the concept: the role of spin effects in oxidases, cytochromes, in dioxygen binding to heme, in photosynthesis, and in tentative models of consciousness. The most thoroughly studied of these effects are connected with dioxygen activation by enzymes. Discussion on the mechanisms of overcoming spin prohibitions in dioxygen reactions with flavin-dependent oxygenases and with hemoglobin and myoglobin is presented in some detail. We consider spin-orbit coupling (SOC) between the starting triplet state from the entrance channel of the O2 binding to glucose oxidase, to ferrous heme, and the final singlet open-shell state in these intermediates. Both triplet (T) and singlet (S) states in these examples are dominated by the radical-pair structures \({\mathrm{D}}^{+}\mbox{ -}{\mathrm{O}}_{2}^{-}\) induced by charge transfer; the peculiarities of their orbital configurations are essential for the SOC analysis. An account of specific SOC in the open πg-shell of dioxygen helps to explain the probability of T-S transitions in the active site near the transition state. Simulated potential energy surface cross-sections along the reaction coordinates for these multiplets, calculated by density functional theory, agree with the notion of a relatively strong SOC induced inside the oxygen moiety by an orbital angular momentum change in the πg-shell during the T-S transition. The SOC model explains well the efficient spin inversion during the O2 binding with heme and glucose oxidase, which constitutes a key mechanism for understanding metabolism. Other examples of nontrivial roles of spin effects in biochemistry are briefly discussed.
Keywords
- Flavin Adenine Dinucleotide
- Spin Transition
- Chemically Induce Dynamic Nuclear Polarization
- Magnetic Perturbation
- Magnetic Field Effect
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Afanasyeva, M. A., Taraban, M. B., Purtov, P. A., Leshina, T. V., & Grissom, C. B. (2006). Magnetic field effects in enzymatic reactions: Radical oxidation of NADH by horseradish peroxidase. Journal of the American Chemical Society, 128, 8651.
Blomberg, M. R. A., Siegbahn, P. E. M., Babcock, G. T., & Wikstrom, M. (2000a). Modeling cytochrome oxidase: A quantum chemical study of the O–O bond cleavage mechanism. Journal of the American Chemical Society, 122, 12848.
Blomberg, M. R. A., Siegbahn, P. E. M., Babcock, G. T., & Wikstrom, M. (2000b). O–O bond splitting mechanism in cytochrome oxidase. Journal of Inorganic Biochemistry, 80, 261.
Blomberg, L. M., Blomberg, M. R. A., & Siegbahn, P. E. M. (2005). A theoretical study of the binding of O2, NO and CO to heme proteins. Journal of Inorganic Biochemistry, 99, 949.
Buchachenko, A. L. (1977). Enrichment of magnetic isotopes–new method of investigation of chemical reaction mechanisms. Russian Journal of Physical Chemistry, 51, 2461.
Buchachenko, A. L., & Kouznetsov, D. A. (2008). Magnetic field affects enzymatic ATP synthesis. Journal of the American Chemical Society, 130, 12868.
Buchachenko, A. L., Kouznetsov, D. A., Orlova, M. A., & Markarian A. A. (2005). Spin biochemistry: Intramitochondrial nucleotide phosphorylation is a magnesium nuclear spin controlled process. Mitochondrion, 5, 67.
Burnold, T. C., & Solomon, E. I. (1999). Reversible dioxygen binding to hemerythrin. Journal of the American Chemical Society, 121, 8288.
Chalkias, N. G., Kahawong, P., & Giannelis E. P. (2008). Activity increase of horseradish peroxidase in the presence of magnetic particles. Journal of the American Chemical Society, 130, 2910.
Davydov, R., Osborne, R. L., Kim, S. H., Dawson, J. H., & Hoffman, B. M. (2008). EPR and ENDOR studies of cryoreduced compound I. Biochemistry, 47, 5147.
de Winter, A., & Boxer, S. G. (2003). Energetics of primary charge separation in bacterial photosynthetic reaction center mutants: Triplet decay in large magnetic field. Journal of Physical Chemistry A, 107, 3341.
Engstrom, M., Minaev, B. F., Vahtras, O., & Agren, H. (1998). MCSCF linear response calculations of electronic g-factor and spin-rotational coupling constants for diatomics. Chemical Physics Letters, 237, 149.
Engstrom, M., Himo, F., Graslund, A., Minaev, B. F., Vahtras, O., & Agren, H. (2000). H-bonding to the tyrosyl radical analyzed by ab initio g-tensor calculations. Journal of Physical Chemistry A, 104, 5149.
Esposito, S. (1999). On the role of spin in quantum mechanics, Foundations of Physics Letters, 12, 165.
Franzen, S. (2002). Spin-dependent mechanism for diatomic ligand binding to heme. Proceedings of the National Academy of Sciences of the United States of America, 99, 16754.
Friedman, J., & Campbell, B. (1987). Structural dynamics and reactivity in hemoglobin. New York: Springer.
Frisch, M. J., Trucks, G. W., Schlegel, H. B., et al. (2003). Gaussian 03, Revision B. 03. Pittsburg: Gaussian Inc.
Gegear, R. J., Conelman, A., & Waddell, S. (2008). Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature, 454, 1014.
Grissom, C. B. (1995). Magnetic field effects in biology: A survey of possible mechanisms with emphasis on radical-pair recombination. Chemical Reviews, 95, 3.
Hagan, S., Hameroff, S. R., & Tuszynski, J. A. (2002). Quantum computation in brain microtubules. Physical Review E, 65, 061901.
Hameroff, S., & Penrose, R. (1996). Conscious events as orchestrated space-time selections. Journal of Consciousness Studies, 3, 36.
Harvey, J. N. (2004). Spin-forbidden CO ligand recombination in myoglobin. Faraday Discussions, 127, 165.
Hoff, A. J. (1986). Magnetic interactions between photosynthetic reactants. Photochemistry and Photobiology, 43, 727.
Hu, H. P., & Wu, M. X. (2004). Spin-mediated consciousness theory. Medical Hypotheses, 63, 633.
Jensen, K. J., & Ryde, U. (2004). How O2 binds to heme. Journal of Biological Chemistry, 279, 14561.
Jensen, K. J., Ross, B. O., & Ryde, U. (2005). The CAS PT2 study of oxymioglobin model. Journal of Inorganic Biochemistry, 99, 45.
Johnsen S., & Lohmann, K. J. (2005). The physics and neurobiology of magnetoreception. Nature Reviews Neuroscience, 6, 703.
Klinman, J. P. (2001). Life as aerobes: Are there simple rules for activation of dioxygen by enzymes? Journal of Biological Inorganic Chemistry, 6, 1.
Kondo, M., & Yoshizawa, K. (2003). A theoretical study of spin-orbit coupling in an Fe(II) spin-crossover complex. Mechanism of the LIESST effect. Chemical Physics Letters, 372, 519.
Kumar, D., de Viser, S. P., Sherma, P. K., Hirao, H., & Shaik, S. (2005). Sulfoxidation mechanisms catalyzed by cytochrome P450 and HRP models: Spin selection induced by the ligand. Biochemistry, 44, 8148.
Lane, N. (2002). Oxygen: The molecule that made the world. Oxford: Oxford University Press.
Maeda, K., Henbest, K. B., Cintolesi, F., Kuprov, I., Rodgers, C. T., Liddell, P. A., Gust, D., Timmel, C. R., & Hore, P. J. (2008). Chemical compass model of avian magnetoreception. Nature, 453, 387.
Metz, M., & Solomon, E. I. (2001). Dioxygen binding to deoxyhemocyanin. Journal of the American Chemical Society, 123, 4938.
Minaev, B. F. (1980). Intensities of spin-forbidden transitions in molecular oxygen. International Journal of Quantum Chemistry, 89, 367.
Minaev, B. F. (1983). Theoretical analysis and prognostication of spin-orbit coupling effects in molecular spectroscopy and chemical kinetics. DrSc Dissertation, Institute of Chemical Physics, Moscow.
Minaev, B. F. (1989). Solvent-induced emission of molecular a1 Δ g oxygen. Journal of Molecular Structure (Theochem), 183, 207.
Minaev, B. F. (2002). Spin effects in reductive activation of O2 by oxidase enzymes. RIKEN Review, 44, 147.
Minaev, B. F. (2004). Ab initio study of the ground state properties of molecular oxygen. Spectrochimica Acta Part A-Molecular and Biomolecular Spectroscopy, 60, 1027.
Minaev, B. F. (2007). Electronic mechanisms of molecular oxygen activation. Russian Chemical Review, 76, 1039.
Minaev, B. F. (2010). Environment friendly spin-catalysis for dioxigen activation. Chemistry & Chemical Technology, 4, 1–16.
Minaev, B. F., & Agren, H. (1995). Spin-orbit coupling induced chemical reactivity and spin-catalysis phenomena. Collection of Czechoslovak Chemical Communications, 60, 339.
Minaev, B. F., & Agren, H. (1996). Spin-catalysis phenomena. International Journal of Quantum Chemistry, 57, 510.
Minaev, B. F., & Ågren, H. (1997). Collision-induced b1 Σ g -a1 Δ g , X3 Σ g -b1 Σ g , and X3 Σ g -a1 Δ g transition probabilities in molecular oxygen. Journal of the Chemical Society-Faraday Transactions, 93, 2231.
Minaev, B. F., & Lunell, S. (1993). Classification of spin-orbit coupling effects in organic chemical reactions. Zeitschrift Fur Physikalische Chemie-International Journal of Research in Physical Chemistry & Chemical Physics, 182, 263.
Minaev, B. F., & Minaev, A. B. (2005). Calculation of the phosphorescence of porphyrins by the density functional method. Optics and Spectroscopy, 98, 214.
Minaev, B. F., & Minaeva, V. A. (2001). MCSCF response calculations of the exited states properties of the O2 molecule and a part of its spectrum. Physical Chemistry Chemical Physics, 3, 720.
Minaev, B. F., Lunell, S., & Kobzev, G. I. (1993). The influence of intermolecular interaction on the forbidden near-IR transitions in molecular oxygen. Journal of Molecular Structure (Theochem), 284, 1.
Minaev, B. F., Mikkelsen, K. V., & Ågren, H. (1997). Collision-induced electronic transitions in complexes between benzene and molecular oxygen. Chemical Physics, 220, 79.
Minaev, B. F., Vahtras, O., & Ågren, H. (1996). Magnetic phosphorescence of molecular oxygen. Chemical Physics, 208, 299.
Minaev, B. F., Lyzhenkova, I. I., Minaeva, V. A., & Boiko, V. I. (1999). A quantum chemical approach to the mechanism of biochemical action of nicotinamide. Theoretical and Experimental Chemistry, 35, 258.
Minaev, B. F., Minaeva, V. A., & Vasenko, O. M. (2007). Spin states of the Fe(II)-pporphin molecule: Quantum-chemical study by DFT method. Ukrainica Bioorganica Acta, 1, 24.
Minaev, B. F., Minaeva, V. A., & Evtuhov, Y. V. (2008). Quantum-chemical study of the singlet oxygen emission. International Journal of Quantum Chemistry, 108, 500.
Ogilby, P. R. (1999). Singlet oxygen. Accounts of Chemical Research, 32, 512.
Orlova, G., Goddard, J. D., & Brovko, L. Y. (2003). Theoretical study of the amazing firefly bioluminescence. Journal of the American Chemical Society, 125, 6962.
Paterson, M. J., Christiansen, O., Jensen, F., & Ogilby, P. R. (2006). Singlet oxygen. Photochemistry and Photobiology, 82, 1136.
Penrose, R. (1960). A spinor approach to general relativity. Annals of Physics, 10, 171.
Penrose, R. (1994). Shadows of the mind. Oxford: Oxford University Press.
Petrich, J. W., Poyart, C., & Martin, J. L. (1988). Spin-forbidden binding of O2 to hemoglobin. Biochemistry, 27, 4049.
Poli, R., & Harvey, J. N. (2003). Spin-forbidden chemical reactions. Chemical Society Reviews, 32, 1.
Potter, W. T., Ticker, M. P., & Caughey, W. S. (1987). Resonance Raman spectra of myoglobin. Biochemistry, 26, 4699.
Prabhakar, R., Siegbahn, P. E. M., Minaev, B. F., & Agren, H. (2002). Activation of triplet dioxygen by glucose oxifase: Spin-orbit coupling in the superoxide ion. Journal of Physical Chemistry B, 106, 3742.
Prabhakar, R., Siegbahn, P. E. M., & Minaev, B. F. (2003). A theoretical study of the dioxygen activation by glucose oxidase and by copper amine oxidase. Biochimica et Biophysica Acta, 1647, 173.
Prabhakar, R., Siegbahn, P. E. M., Minaev, B. F., & Agren, H. (2004). Spin transition during H2O2 formation in the oxidative half-reaction of copper amine oxidase. Journal of Physical Chemistry B, 108, 13882.
Sawyer, D. T. (1991). Oxygen chemistry. New York: Oxford University.
Schweitzer, C., & Schmidt, R. (2003). Physical mechanisms of generation and deactivation of singlet oxygen. Chemical Reviews, 103, 1685.
Serebrennikov, Y. A., & Minaev, B. F. (1987). Magnetic field effects due to spin-orbit coupling in transient intermediates. Chemical Physics, 114, 359.
Shaik, S., Filatov, M., Schroder, D., & Schvarz, H. (1998). Electronic structure makes a difference: Cytochrome P-450 mediated hydroxylation of hydrocarbons as a two-state reactivity paradigm. Chemistry-A European Journal, 4, 193.
Shaik, S., Ogliaro, F., de Visser, S. P., Schwarz, H., & Schroeder, D. (2002). Two state reactivity mechanism of hydroxylation and epoxidation by cytochrome P450 revealed by theory. Current Opinion in Chemical Biology, 6, 556.
Shaik, S., Kumar, D., de Viser, S. P., Altun, A., & Tiel, W. (2005). Theoretical perspective on the structure of cytochrome P450 enzymes. Chemical Reviews, 105, 2279.
Sheldon, R. A. (1993). A history of oxygen activation. In D. Barton et al. (Eds.), The Activation of dioxygen and homogeneous catalytic oxidation. New York: Plenum.
Shikama, K. (2006). Nature of the FeO2 bonding in myoglobin and hemoglobin. A new molecular paradigm. Progress in Biophysics and Molecular Biology, 91, 83.
Sigfridsson, E., & Ryde, U. (2002). Theoretical study of discrimination between O2 and CO by myoglobin. Journal of Inorganic Chemistry, 91, 101.
Silva, P. J., & Ramos, M. J. (2008). A comparative DFT study of the reaction mechanism of the O2-depemdemt coproporphyrinogen III oxidase. Bioorganic Medical Chemistry, 16, 2726.
Strickland, N., & Harwey, J. N. (2007). Spin-forbidden ligand binding to the ferrous-heme group. Journal of Physical Chemistry B, 111, 841.
Stryer, L. (1995). Biochemistry (4th ed., p. 152). New York: Freeman.
Acknowledgments
This work is supported by the State Foundation of Fundamental Investigations (DFFD) of Ukraine, the project F25.5/008, and by Visby project No = 01403/2007.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media B.V.
About this entry
Cite this entry
Minaev, B.F., Minaeva, V.O., Ågren, H. (2012). Spin-Orbit Coupling in Enzymatic Reactions and the Role of Spin in Biochemistry. In: Leszczynski, J. (eds) Handbook of Computational Chemistry. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0711-5_29
Download citation
DOI: https://doi.org/10.1007/978-94-007-0711-5_29
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0710-8
Online ISBN: 978-94-007-0711-5
eBook Packages: Chemistry and Materials ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics