[en] A multidimensional quantum mechanical protocol
is used to describe the photoinduced electron transfer
and electronic coherence in plant cryptochromes without any
semiempirical, e.g., experimentally obtained, parameters.
Starting from a two-level spin-boson Hamiltonian we look at
the effect that the initial photoinduced nuclear bath distribution has on an intermediate step of this biological electron transfer cascade for two idealized cases. The first assumes a slow equilibration of the nuclear bath with respect to the previous electron transfer step that leads to an ultrafast decay with little temperature dependence; while the second assumes a prior fast bath equilibration on the donor potential energy surface leading to a much slower decay, which contrarily displays a high temperature dependence and a better agreement with previous theoretical and experimental results. Beyond Marcus and semiclassical pictures these results unravel the strong impact that the presence or not of equilibrium initial conditions has on the electronic population and coherence dynamics at the quantum dynamics level in this and conceivably in other biological electron transfer cascades.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Romero, E.; Augulis, R.; Novoderezhkin, V. I.; Ferretti, M.; Thieme, J.; Zigmantas, D.; van Grondelle, R. Quantum coherence in photosynthesis for efficient solar-energy conversion Nat. Phys. 2014, 10, 676-682 10.1038/nphys3017
Engel, G. S.; Calhoun, T. R.; Read, E. L.; Ahn, T.-K.; Mancal, T.; Cheng, Y.-C.; Blankenship, R. E.; Fleming, G. R. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems Nature 2007, 446, 782-786 10.1038/nature05678
Scholes, G. D.; Fleming, G. R.; Chen, L. X.; Aspuru-Guzik, A.; Buchleitner, A.; Coker, D. F.; Engel, G. S.; van Grondelle, R.; Ishizaki, A.; Jonas, D. M. et al. Using coherence to enhance function in chemical and biophysical systems Nature 2017, 543, 647-656 10.1038/nature21425
de la Lande, A.; Cailliez, F.; Salahub, D. R. Simulating Enzyme Reactivity: Computational Methods in Enzyme Catalysis; The Royal Society of Chemistry, 2017; pp 89-149.
Michael, A. K.; Fribourgh, J. L.; van Gelder, R. N.; Partch, C. L. Animal Cryptochromes: Divergent Roles in Light Perception, Circadian Timekeeping and Beyond Photochem. Photobiol. 2017, 93, 128-140 10.1111/php.12677
Chaves, I.; Pokorny, R.; Byrdin, M.; Hoang, N.; Ritz, T.; Brettel, K.; Essen, L. O.; van der Horst, G. T. J.; Batschauer, A.; Ahmad, M. The Cryptochromes: Blue Light Photoreceptors in Plants and Animals Annu. Rev. Plant Biol. 2011, 62, 335-364 10.1146/annurev-arplant-042110-103759
Hore, P. J.; Mouritsen, H. The Radical-Pair Mechanism of Magnetoreception Annu. Rev. Biophys. 2016, 45, 299-344 10.1146/annurev-biophys-032116-094545
Kattnig, D. R.; Evans, E. W.; Déjean, V.; Dodson, C. A.; Wallace, M. I.; Mackenzie, S. R.; Timmel, C. R.; Hore, P. J. Chemical amplification of magnetic field effects relevant to avian magnetoreception Nat. Chem. 2016, 8, 384-391 10.1038/nchem.2447
Hiscock, H. G.; Worster, S.; Kattnig, D. R.; Steers, C.; Jin, Y.; Manolopoulos, D. E.; Mouritsen, H.; Hore, P. J. The quantum needle of the avian magnetic compass Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 4634-4639 10.1073/pnas.1600341113
Maeda, K.; Robinson, A. J.; Henbest, K. B.; Hogben, H. J.; Biskup, T.; Ahmad, M.; Schleicher, E.; Weber, S.; Timmel, C. R.; Hore, P. J. Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 4774-4779 10.1073/pnas.1118959109
Ritz, T.; Adem, S.; Schulten, K. A Model for Photoreceptor-Based Magnetoreception in Birds Biophys. J. 2000, 78, 707-718 10.1016/S0006-3495(00)76629-X
Solov'yov, I. A.; Chandler, D. E.; Schulten, K. Magnetic Field Effects in Arabidopsis thaliana Cryptochrome-1 Biophys. J. 2007, 92, 2711-2726 10.1529/biophysj.106.097139
Schulten, K.; Swenberg, C. E.; Weller, A. Biomagnetic sensory mechanism based on magnetic-field modulated coherent electron-spin motion Z. Phys. Chem. 1978, 111, 1-5 10.1524/zpch.1978.111.1.001
Immeln, D.; Weigel, A.; Kottke, T.; Pérez Lustres, J. L. Primary Events in the Blue Light Sensor Plant Cryptochrome: Intraprotein Electron and Proton Transfer Revealed by Femtosecond Spectroscopy J. Am. Chem. Soc. 2012, 134, 12536-12546 10.1021/ja302121z
Firmino, T.; Mangaud, E.; Cailliez, F.; Devolder, A.; Mendive-Tapia, D.; Gatti, F.; Meier, C.; Desouter-Lecomte, M.; de la Lande, A. Quantum effects in ultrafast electron transfers within cryptochromes Phys. Chem. Chem. Phys. 2016, 18, 21442-21457 10.1039/C6CP02809H
Cailliez, F.; Müller, P.; Gallois, M.; de la Lande, A. ATP Binding and Aspartate Protonation Enhance Photoinduced Electron Transfer in Plant Cryptochrome J. Am. Chem. Soc. 2014, 136, 12974-12986 10.1021/ja506084f
Lüdemann, G.; Solov'yov, I. A.; Kubař, T.; Elstner, M. Solvent Driving Force Ensures Fast Formation of a Persistent and Well-Separated Radical Pair in Plant Cryptochrome J. Am. Chem. Soc. 2015, 137, 1147-1156 10.1021/ja510550g
de la Lande, A.; Salahub, D. R. Derivation of interpretative models for long range electron transfer from constrained density functional theory J. Mol. Struct.: THEOCHEM 2010, 943, 115-120 10.1016/j.theochem.2009.11.012
Carrillo, A.; Cornelio, M. F.; de Oliveira, M. C. Environment-induced anisotropy and sensitivity of the radical pair mechanism in the avian compass Phys. Rev. E 2015, 92, 012720 10.1103/PhysRevE.92.012720
Poonia, V. S.; Saha, D.; Ganguly, S. State transitions and decoherence in the avian compass Phys. Rev. E 2015, 91, 052709 10.1103/PhysRevE.91.052709
Walters, Z. B. Quantum dynamics of the avian compass Phys. Rev. E 2014, 90, 042710 10.1103/PhysRevE.90.042710
Bandyopadhyay, J. N.; Paterek, T.; Kaszlikowski, D. Quantum Coherence and Sensitivity of Avian Magnetoreception Phys. Rev. Lett. 2012, 109, 110502 10.1103/PhysRevLett.109.110502
Cai, J.; Caruso, F.; Plenio, M. B. Quantum limits for the magnetic sensitivity of a chemical compass Phys. Rev. A: At., Mol., Opt. Phys. 2012, 85, 040304 10.1103/PhysRevA.85.040304
Lau, J. C. S.; Wagner-Rundell, N.; Rodgers, C. T.; Green, N. J. B.; Hore, P. J. Effects of disorder and motion in a radical pair magnetoreceptor J. R. Soc., Interface 2010, 7, S257 10.1098/rsif.2009.0399.focus
de la Lande, A.; Gillet, N.; Chen, S.; Salahub, D. R. Progress and challenges in simulating and understanding electron transfer in proteins Arch. Biochem. Biophys. 2015, 582, 28-41 10.1016/j.abb.2015.06.016
Kattnig, D. R.; Solov'yov, I. A.; Hore, P. J. Electron spin relaxation in cryptochrome-based magnetoreception Phys. Chem. Chem. Phys. 2016, 18, 12443-12456 10.1039/C5CP06731F
Tavernelli, I. Nonadiabatic Molecular Dynamics Simulations: Synergies between Theory and Experiments Acc. Chem. Res. 2015, 48, 792-800 10.1021/ar500357y
Persico, M.; Granucci, G. An overview of nonadiabatic dynamics simulations methods, with focus on the direct approach versus the fitting of potential energy surfaces Theor. Chem. Acc. 2014, 133, 1526 10.1007/s00214-014-1526-1
Feynman, R.; Vernon, F. The theory of a general quantum system interacting with a linear dissipative system Ann. Phys. 1963, 24, 118-173 10.1016/0003-4916(63)90068-X
Xu, R.-X.; Yan, Y. Dynamics of quantum dissipation systems interacting with bosonic canonical bath: Hierarchical equations of motion approach Phys. Rev. E 2007, 75, 031107 10.1103/PhysRevE.75.031107
Tanimura, Y. Stochastic Liouville, Langevin, Fokker-Planck, and Master Equation Approaches to Quantum Dissipative Systems J. Phys. Soc. Jpn. 2006, 75, 082001 10.1143/JPSJ.75.082001
Ishizaki, A.; Tanimura, Y. Quantum Dynamics of System Strongly Coupled to Low-Temperature Colored Noise Bath: Reduced Hierarchy Equations Approach J. Phys. Soc. Jpn. 2005, 74, 3131-3134 10.1143/JPSJ.74.3131
Tanimura, Y.; Kubo, R. Time Evolution of a Quantum System in Contact with a Nearly Gaussian-Markoffian Noise Bath J. Phys. Soc. Jpn. 1989, 58, 101-114 10.1143/JPSJ.58.101
Meyer, H.-D. Studying molecular quantum dynamics with the multiconfiguration time-dependent Hartree method WIREs: Comput. Mol. Sci. 2012, 2, 351-374 10.1002/wcms.87
Wang, H.; Thoss, M. From coherent motion to localization: dynamics of the spin-boson model at zero temperature New J. Phys. 2008, 10, 115005 10.1088/1367-2630/10/11/115005
Thoss, M.; Wang, H.; Miller, W. H. Self-consistent hybrid approach for complex systems: Application to the spin-boson model with Debye spectral density J. Chem. Phys. 2001, 115, 2991-3005 10.1063/1.1385562
Ashkenazi, G.; Kosloff, R.; Ratner, M. A. Photoexcited Electron Transfer: Short-Time Dynamics and Turnover Control by Dephasing, Relaxation, and Mixing J. Am. Chem. Soc. 1999, 121, 3386-3395 10.1021/ja981998p
Ando, K.; Sumi, H. Nonequilibrium Oscillatory Electron Transfer in Bacterial Photosynthesis J. Phys. Chem. B 1998, 102, 10991-11000 10.1021/jp982659l
Kühn, O.; May, V.; Schreiber, M. Dissipative vibrational dynamics in a curve-crossing system J. Chem. Phys. 1994, 101, 10404-10415 10.1063/1.467921
Coalson, R. D.; Evans, D. G.; Nitzan, A. A nonequilibrium golden rule formula for electronic state populations in nonadiabatically coupled systems J. Chem. Phys. 1994, 101, 436-448 10.1063/1.468153
Xu, D.; Schulten, K. Coupling of protein motion to electron transfer in a photosynthetic reaction center: investigating the low temperature behavior in the framework of the spin-boson model Chem. Phys. 1994, 182, 91-117 10.1016/0301-0104(94)00016-6
Schneider, R.; Domcke, W.; Köppel, H. Aspects of dissipative electronic and vibrational dynamics of strongly vibronically coupled systems J. Chem. Phys. 1990, 92, 1045-1061 10.1063/1.458167
Garg, A.; Onuchic, J. N.; Ambegaokar, V. Effect of friction on electron transfer in biomolecules J. Chem. Phys. 1985, 83, 4491-4503 10.1063/1.449017
Tamura, H.; Martinazzo, R.; Ruckenbauer, M.; Burghardt, I. Quantum dynamics of ultrafast charge transfer at an oligothiophene-fullerene heterojunction J. Chem. Phys. 2012, 137, 22A540 10.1063/1.4751486
Tamura, H.; Burghardt, I.; Tsukada, M. Exciton Dissociation at Thiophene/Fullerene Interfaces: The Electronic Structures and Quantum Dynamics J. Phys. Chem. C 2011, 115, 10205-10210 10.1021/jp203174e
Řezáč, J.; Lévy, B.; Demachy, I.; de la Lande, A. Robust and Efficient Constrained DFT Molecular Dynamics Approach for Biochemical Modeling J. Chem. Theory Comput. 2012, 8, 418-427 10.1021/ct200570u
Valleau, S.; Eisfeld, A.; Aspuru-Guzik, A. On the alternatives for bath correlators and spectral densities from mixed quantum-classical simulations J. Chem. Phys. 2012, 137, 224103 10.1063/1.4769079
Shi, Q.; Chen, L.; Nan, G.; Xu, R.-X.; Yan, Y. Efficient hierarchical Liouville space propagator to quantum dissipative dynamics J. Chem. Phys. 2009, 130, 084105 10.1063/1.3077918
Pomyalov, A.; Meier, C.; Tannor, D. The importance of initial correlations in rate dynamics: A consistent non-Markovian master equation approach Chem. Phys. 2010, 370, 98-108 10.1016/j.chemphys.2010.02.017
Meier, C.; Tannor, D. J. Non-Markovian evolution of the density operator in the presence of strong laser fields J. Chem. Phys. 1999, 111, 3365-3376 10.1063/1.479669
Vacher, M.; Meisner, J.; Mendive-Tapia, D.; Bearpark, M. J.; Robb, M. A. Electronic Control of Initial Nuclear Dynamics Adjacent to a Conical Intersection J. Phys. Chem. A 2015, 119, 5165-5172 10.1021/jp509774t
Vacher, M.; Mendive-Tapia, D.; Bearpark, M. J.; Robb, M. A. Electron dynamics upon ionization: Control of the timescale through chemical substitution and effect of nuclear motion J. Chem. Phys. 2015, 142, 094105 10.1063/1.4913515
Vacher, M.; Albertani, F. E. A.; Jenkins, A. J.; Polyak, I.; Bearpark, M. J.; Robb, M. A. Electron and nuclear dynamics following ionisation of modified bismethylene-adamantane Faraday Discuss. 2016, 194, 95-115 10.1039/C6FD00067C
Blancafort, L.; Hunt, P.; Robb, M. A. Intramolecular Electron Transfer in Bis(methylene) Adamantyl Radical Cation: A Case Study of Diabatic Trapping J. Am. Chem. Soc. 2005, 127, 3391-3399 10.1021/ja043879h
Mendive-Tapia, D.; Kortekaas, L.; Steen, J. D.; Perrier, A.; Lasorne, B.; Browne, W. R.; Jacquemin, D. Accidental degeneracy in the spiropyran radical cation: charge transfer between two orthogonal rings inducing ultra-efficient reactivity Phys. Chem. Chem. Phys. 2016, 18, 31244-31253 10.1039/C6CP06907J
Blancafort, L.; Jolibois, F.; Olivucci, M.; Robb, M. A. Potential Energy Surface Crossings and the Mechanistic Spectrum for Intramolecular Electron Transfer in Organic Radical Cations J. Am. Chem. Soc. 2001, 123, 722-732 10.1021/ja003359w
Worth, G. A.; Beck, M. H.; Jäckle, A.; Vendrell, O.; Meyer, H.-D. The MCTDH Package, Version 8.2, (2000). H.-D. Meyer, Version 8.3 (2002), Version 8.4 (2007). O. Vendrell and H.-D. Meyer Version 8.5 (2013). Version 8.5 contains the ML-MCTDH algorithm. Current versions: 8.4.12 and 8.5.5 (2016). See http://mctdh.uni-hd.de (accessed Dec 7, 2017).
Multidimensional Quantum Dynamics: MCTDH Theory and Applications; Meyer, H.-D.; Gatti, F.; Worth, G. A., Eds.; Wiley-VCH: Weinheim, 2009.
Meyer, H.-D.; Worth, G. A. Quantum molecular dynamics: Propagating wavepackets and density operators using the multiconfiguration time-dependent Hartree (MCTDH) method Theor. Chem. Acc. 2003, 109, 251-267 10.1007/s00214-003-0439-1
Beck, M. H.; Jäckle, A.; Worth, G. A.; Meyer, H.-D. The multi-configuration time-dependent Hartree (MCTDH) method: A highly efficient algorithm for propagating wave packets Phys. Rep. 2000, 324, 1-105 10.1016/S0370-1573(99)00047-2
Manthe, U.; Meyer, H.-D.; Cederbaum, L. S. Wave-Packet Dynamics within the Multiconfiguration Hartree Framework: General Aspects and application to NOCl J. Chem. Phys. 1992, 97, 3199-3213 10.1063/1.463007
Meyer, H.-D.; Manthe, U.; Cederbaum, L. S. The Multi-Configurational Time-Dependent Hartree Approach Chem. Phys. Lett. 1990, 165, 73-78 10.1016/0009-2614(90)87014-I
Schulze, J.; Shibl, M. F.; Al-Marri, M. J.; Kühn, O. Multi-layer multi-configuration time-dependent Hartree (ML-MCTDH) approach to the correlated exciton-vibrational dynamics in the FMO complex J. Chem. Phys. 2016, 144, 185101 10.1063/1.4948563
Schulze, J.; Kühn, O. Explicit Correlated Exciton-Vibrational Dynamics of the FMO Complex J. Phys. Chem. B 2015, 119, 6211-6216 10.1021/acs.jpcb.5b03928
Nest, M.; Kosloff, R. Quantum dynamical treatment of inelastic scattering of atoms at a surface at finite temperature: The random phase thermal wave function approach J. Chem. Phys. 2007, 127, 134711 10.1063/1.2786088
Gelman, D.; Kosloff, R. Simulating dissipative phenomena with a random phase thermal wavefunctions, high temperature application of the Surrogate Hamiltonian approach Chem. Phys. Lett. 2003, 381, 129-138 10.1016/j.cplett.2003.09.119
Mendive-Tapia, D.; Firmino, T.; Meyer, H.-D.; Gatti, F. Towards a systematic convergence of Multi-Layer (ML) Multi-Configuration Time-Dependent Hartree nuclear wavefunctions: The ML-spawning algorithm Chem. Phys. 2017, 482, 113-123 10.1016/j.chemphys.2016.08.031
Kreisbeck, C.; Kramer, T. Long-Lived Electronic Coherence in Dissipative Exciton Dynamics of Light-Harvesting Complexes J. Phys. Chem. Lett. 2012, 3, 2828-2833 10.1021/jz3012029
Bizzarri, A. R.; Cannistraro, S. Molecular Dynamics of Water at the Protein-Solvent Interface J. Phys. Chem. B 2002, 106, 6617-6633 10.1021/jp020100m
Joti, Y.; Kitao, A.; Go, N. Protein Boson Peak Originated from Hydration-Related Multiple Minima Energy Landscape J. Am. Chem. Soc. 2005, 127, 8705-8709 10.1021/ja0425886
Cailliez, F.; Müller, P.; Firmino, T.; Pernot, P.; de la Lande, A. Energetics of Photoinduced Charge Migration within the Tryptophan Tetrad of an Animal (6-4) Photolyase J. Am. Chem. Soc. 2016, 138, 1904-1915 10.1021/jacs.5b10938
Woiczikowski, P. B.; Steinbrecher, T.; Kubař, T.; Elstner, M. Nonadiabatic QM/MM Simulations of Fast Charge Transfer in Escherichia coli DNA Photolyase J. Phys. Chem. B 2011, 115, 9846-9863 10.1021/jp204696t
Qin, Y.; Wang, L.; Zhong, D. Dynamics and mechanism of ultrafast water-protein interactions Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 8424-8429 10.1073/pnas.1602916113
Li, T.; Hassanali, A. A.; Kao, Y.-T.; Zhong, D.; Singer, S. J. Hydration Dynamics and Time Scales of Coupled Water-Protein Fluctuations J. Am. Chem. Soc. 2007, 129, 3376-3382 10.1021/ja0685957
Zhang, L.; Wang, L.; Kao, Y.-T.; Qiu, W.; Yang, Y.; Okobiah, O.; Zhong, D. Mapping hydration dynamics around a protein surface Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 18461-18466 10.1073/pnas.0707647104
Decleva, P.; Quadri, N.; Perveaux, A.; Lauvergnat, D.; Gatti, F.; Lasorne, B.; Halász, G. J.; Vibók, á. Attosecond electronic and nuclear quantum photodynamics of ozone monitored with time and angle resolved photoelectron spectra Sci. Rep. 2016, 6, 36613 10.1038/srep36613
Mendive-Tapia, D.; Vacher, M.; Bearpark, M. J.; Robb, M. A. Coupled electron-nuclear dynamics: Charge migration and charge transfer initiated near a conical intersection J. Chem. Phys. 2013, 139, 044110 10.1063/1.4815914
Cederbaum, L.; Zobeley, J. Ultrafast charge migration by electron correlation Chem. Phys. Lett. 1999, 307, 205-210 10.1016/S0009-2614(99)00508-4
Arnold, C.; Vendrell, O.; Santra, R. Electronic decoherence following photoionization: Full quantum-dynamical treatment of the influence of nuclear motion Phys. Rev. A: At., Mol., Opt. Phys. 2017, 95, 033425 10.1103/PhysRevA.95.033425
Vacher, M.; Bearpark, M. J.; Robb, M. A.; Malhado, J. a. P. Electron Dynamics upon Ionization of Polyatomic Molecules: Coupling to Quantum Nuclear Motion and Decoherence Phys. Rev. Lett. 2017, 118, 083001 10.1103/PhysRevLett.118.083001
Despré, V.; Marciniak, A.; Loriot, V.; Galbraith, M. C. E.; Rouzée, A.; Vrakking, M. J. J.; Lépine, F.; Kuleff, A. I. Attosecond Hole Migration in Benzene Molecules Surviving Nuclear Motion J. Phys. Chem. Lett. 2015, 6, 426-431 10.1021/jz502493j
Nisoli, M.; Decleva, P.; Calegari, F.; Palacios, A.; Martln, F. Attosecond Electron Dynamics in Molecules Chem. Rev. 2017, 117, 10760 10.1021/acs.chemrev.6b00453
Lepine, F.; Ivanov, M. Y.; Vrakking, M. J. J. Attosecond molecular dynamics: fact or fiction? Nat. Photonics 2014, 8, 195-204 10.1038/nphoton.2014.25
Kuleff, A. I.; Cederbaum, L. S. Ultrafast correlation-driven electron dynamics J. Phys. B: At., Mol. Opt. Phys. 2014, 47, 124002 10.1088/0953-4075/47/12/124002
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
