A quantum chemical perspective of photoactivated biological functions
-
Benedetta Mennucci
Abstract
Quantum chemistry plays a fundamental role in unraveling the mechanisms by which biological systems sense and use light, driving functions such as light harvesting and energy conversion, and photoreception and signaling. In this Perspective, we first present the fundamental physical principles underlying the light-induced biological functions. We then focus on the key theoretical frameworks and multiscale modeling strategies based on quantum chemistry that enable a detailed, atomistic description of the processes initiating the biological response to light. Special emphasis is placed on three fundamental photophysical and photochemical processes (excitation energy transfer, photochemical reactions, and electron transfer) which form the core of photoactivation mechanisms in biological systems. By highlighting the advances and challenges associated with the quantum chemical modeling, we demonstrate its essential contribution to deepening our understanding of photoinduced biological function and point to future directions for methodological innovation.
-
Research ethics: Not applicable.
-
Informed consent: Not applicable.
-
Author contributions: The author has accepted responsibility for the entire content of this manuscript and approved its submission.
-
Use of Large Language Models, AI and Machine Learning Tools: None declared.
-
Conflict of interest: The author states no conflict of interest.
-
Research funding: None declared.
-
Data availability: Not applicable.
References
1. Senn, H. M.; we QM/MM Methods for Biomolecular Systems. Angew. Chem. Int. Ed. 2009, 48, 1198–1229; https://doi.org/10.1002/anie.200802019.Suche in Google Scholar PubMed
2. Brunk, E.; Rothlisberger, U. Mixed Quantum Mechanical/Molecular Mechanical Molecular Dynamics Simulations of Biological Systems in Ground and Electronically Excited States. Chem. Rev. 2015, 115, 6217–6263; https://doi.org/10.1021/cr500628b.Suche in Google Scholar PubMed
3. Boulanger, E.; Harvey, J. N. QM/MM Methods for Free Energies and Photochemistry. Curr. Opin. Struct. Biol. 2018, 49, 72–76; https://doi.org/10.1016/j.sbi.2018.01.003.Suche in Google Scholar PubMed
4. Mennucci, B.; Corni, S. Multiscale Modelling of Photoinduced Processes in Composite Systems. Nat. Rev. Chem. 2019, 3, 315–330; https://doi.org/10.1038/s41570-019-0092-4.Suche in Google Scholar
5. Bondanza, M.; Nottoli, M.; Cupellini, L.; Lipparini, F.; Mennucci, B. Polarizable Embedding QM/MM: the Future Gold Standard for Complex (Bio)Systems? Phys. Chem. Chem. Phys. 2020, 22, 14433–14448; https://doi.org/10.1039/d0cp02119a.Suche in Google Scholar PubMed
6. Nottoli, M.; Cupellini, L.; Lipparini, F.; Granucci, G.; Mennucci, B. Multiscale Models for Light-Driven Processes. Annu. Rev. Phys. Chem. 2021, 72, 1–25; https://doi.org/10.1146/annurev-physchem-090419-104031.Suche in Google Scholar PubMed
7. Kubař, T.; Elstner, M.; Cui, Q. Hybrid Quantum Mechanical/Molecular Mechanical Methods for Studying Energy Transduction in Biomolecular Machines. Annu. Rev. Biophys. 2023, 52, 525–551; https://doi.org/10.1146/annurev-biophys-111622-091140.Suche in Google Scholar PubMed PubMed Central
8. Carrasco-Busturia, D.; Ippoliti, E.; Meloni, S.; Rothlisberger, U.; Olsen, J. M. H. Multiscale Biomolecular Simulations in the Exascale Era. Curr. Opin. Struct. Biol. 2024, 86, 102821; https://doi.org/10.1016/j.sbi.2024.102821.Suche in Google Scholar PubMed
9. Avagliano, D.; Conti, I.; El-Tahawy, M. M.; Jaiswal, V. K.; Nenov, A.; Garavelli, M. In Comprehensive Computational Chemistry; Yáñez, M.; Boyd, R. J., Eds.; Elsevier: Oxford, 2024, 1st ed.; pp. 158–187.10.1016/B978-0-12-821978-2.00059-3Suche in Google Scholar
10. Acharya, A.; Bogdanov, A. M.; Grigorenko, B. L.; Bravaya, K. B.; Nemukhin, A. V.; Lukyanov, K. A.; Krylov, A. I. Photoinduced Chemistry in Fluorescent Proteins: Curse or Blessing? Chem. Rev. 2017, 117, 758–795; https://doi.org/10.1021/acs.chemrev.6b00238.Suche in Google Scholar PubMed
11. Mroginski, M. A.; Adam, S.; Amoyal, G. S.; Barnoy, A.; Bondar, A.; Borin, V. A.; Church, J. R.; Domratcheva, T.; Ensing, B.; Fanelli, F.; Ferré, N.; Filiba, O.; Pedraza-González, L.; González, R.; González-Espinoza, C. E.; Kar, R. K.; Kemmler, L.; Kim, S. S.; Kongsted, J.; Krylov, A. I.; Lahav, Y.; Lazaratos, M.; NasserEddin, Q.; Navizet, I.; Nemukhin, A.; Olivucci, M.; Olsen, J. M. H.; Pérez de Alba Ortíz, A.; Pieri, E.; Rao, A. G.; Rhee, Y. M.; Ricardi, N.; Sen, S.; Solov’yov, I. A.; De Vico, L.; Wesolowski, T. A.; Wiebeler, C.; Yang, X.; Schapiro, I. Frontiers in Multiscale Modeling of Photoreceptor Proteins. Photochem. Photobiol. 2021, 97, 243–269; https://doi.org/10.1111/php.13372.Suche in Google Scholar PubMed PubMed Central
12. Salvadori, G.; Mazzeo, P.; Accomasso, D.; Cupellini, L.; Mennucci, B. Deciphering Photoreceptors Through Atomistic Modeling from Light Absorption to Conformational Response. J. Mol. Biol. 2024, 436, 168358; https://doi.org/10.1016/j.jmb.2023.168358.Suche in Google Scholar PubMed
13. Croce, R.; van Amerongen, H. Natural Strategies for Photosynthetic Light Harvesting. Nat. Chem. Biol. 2014, 10, 492–501; https://doi.org/10.1038/nchembio.1555.Suche in Google Scholar PubMed
14. Mirkovic, T.; Ostroumov, E. E.; Anna, J. M.; van Grondelle, R.; Govindjee; Scholes, G. D. Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms. Chem. Rev. 2017, 117, 249–293; https://doi.org/10.1021/acs.chemrev.6b00002.Suche in Google Scholar PubMed
15. Blankenship, R. E. Molecular Mechanisms of Photosynthesis; John Wiley & Sons: Chichester, UK, 2014.Suche in Google Scholar
16. Kottke, T.; Xie, A.; Larsen, D. S.; Hoff, W. D. Photoreceptors Take Charge: Emerging Principles for Light Sensing. Annu. Rev. Biophys. 2018, 47, 1–23; https://doi.org/10.1146/annurev-biophys-070317-033047.Suche in Google Scholar PubMed
17. Christie, J. M.; Blackwood, L.; Petersen, J.; Sullivan, S. Plant Flavoprotein Photoreceptors. Plant Cell Physiol. 2015, 56, 401–413; https://doi.org/10.1093/pcp/pcu196.Suche in Google Scholar PubMed PubMed Central
18. Wang, J.; Du, X.; Pan, W.; Wang, X.; Wu, W. Photoactivation of the Cryptochrome/Photolyase Superfamily. Reviews J. Photochem. Photobiol. C Photochem. Rev. 2015, 22, 84–102; https://doi.org/10.1016/j.jphotochemrev.2014.12.001.Suche in Google Scholar
19. Kennis, J. T. M.; Mathes, T. Molecular Eyes: Proteins that Transform Light into Biological Information. Interface Focus 2013, 3, 20130005–13; https://doi.org/10.1098/rsfs.2013.0005.Suche in Google Scholar PubMed PubMed Central
20. Runda, M. E.; Schmidt, S. Light-Driven Bioprocesses. Phys. Sci. Rev. 2023, 9, 2287–2320; https://doi.org/10.1515/psr-2022-0109.Suche in Google Scholar
21. Taylor, A.; Heyes, D. J.; Scrutton, N. S. Catalysis by Nature’s Photoenzymes. Curr. Opin. Struct. Biol. 2022, 77, 102491; https://doi.org/10.1016/j.sbi.2022.102491.Suche in Google Scholar PubMed
22. Caffarri, S.; Kouřil, R.; Kereïche, S.; Boekema, E. J.; Croce, R. Functional Architecture of Higher Plant Photosystem II Supercomplexes. EMBO J. 2009, 28, 3052–3063; https://doi.org/10.1038/emboj.2009.232.Suche in Google Scholar PubMed PubMed Central
23. Shevela, D.; Kern, J. F.; Govindjee, G.; Messinger, J. Solar Energy Conversion by Photosystem II: Principles and Structures. Photosynth. Res. 2023, 156, 279–307; https://doi.org/10.1007/s11120-022-00991-y.Suche in Google Scholar PubMed PubMed Central
24. Iwai, M.; Patel-Tupper, D.; Niyogi, K. K. Structural Diversity in Eukaryotic Photosynthetic Light Harvesting. Annu. Rev. Plant Biol. 2024, 75, 120–152; https://doi.org/10.1146/annurev-arplant-070623-015519.Suche in Google Scholar PubMed
25. Son, M.; Hart, S. M.; Schlau-Cohen, G. S. Investigating Carotenoid Photophysics in Photosynthesis with 2D Electronic Spectroscopy. Trends Chem. 2021, 3, 733–746; https://doi.org/10.1016/j.trechm.2021.05.008.Suche in Google Scholar
26. Collini, E. Carotenoids in Photosynthesis: The Revenge of the “Accessory” Pigments. Chem 2019, 5, 494–495; https://doi.org/10.1016/j.chempr.2019.02.013.Suche in Google Scholar
27. Niyogi, K. K.; Truong, T. B. Evolution of Flexible Non-photochemical Quenching Mechanisms that Regulate Light Harvesting in Oxygenic Photosynthesis. Curr. Opin. Plant Biol. 2013, 16, 307–314; https://doi.org/10.1016/j.pbi.2013.03.011.Suche in Google Scholar PubMed
28. Pinnola, A.; Bassi, R. Molecular Mechanisms Involved in Plant Photoprotection. Biochem. Soc. Trans. 2018, 46, 467–482; https://doi.org/10.1042/bst20170307.Suche in Google Scholar PubMed
29. Murchie, E. H.; Ruban, A. V. Dynamic Non-photochemical Quenching in Plants: from Molecular Mechanism to Productivity. Plant J. 2020, 101, 885–896; https://doi.org/10.1111/tpj.14601.Suche in Google Scholar PubMed
30. Sirohiwal, A.; Pantazis, D. A. Reaction Center Excitation in Photosystem II: From Multiscale Modeling to Functional Principles. Acc. Chem. Res. 2023, 56, 2921–2932; https://doi.org/10.1021/acs.accounts.3c00392.Suche in Google Scholar PubMed PubMed Central
31. Tamura, H.; Saito, K.; Ishikita, H. The Origin of Unidirectional Charge Separation in Photosynthetic Reaction Centers: Nonadiabatic Quantum Dynamics of Exciton and Charge in Pigment–Protein Complexes. Chem. Sci. 2021, 12, 8131–8140; https://doi.org/10.1039/d1sc01497h.Suche in Google Scholar PubMed PubMed Central
32. Capone, M.; Sirohiwal, A.; Aschi, M.; Pantazis, D. A.; Daidone, I. Alternative Fast and Slow Primary Charge-Separation Pathways in Photosystem II. Angew. Chem., Int. Ed. 2023, 62, e202216276; https://doi.org/10.1002/anie.202216276.Suche in Google Scholar PubMed
33. Forde, A.; Maity, S.; Freixas, V. M.; Fernandez-Alberti, S.; Neukirch, A. J.; Kleinekathöfer, U.; Tretiak, S. Stabilization of Charge-Transfer Excited States in Biological Systems: A Computational Focus on the Special Pair in Photosystem II Reaction Centers. J. Phys. Chem. Lett. 2024, 15, 4142–4150; https://doi.org/10.1021/acs.jpclett.4c00362.Suche in Google Scholar PubMed
34. Rockwell, N. C.; Su, Y.-S.; Lagarias, J. C. Phytochrome Structure and Signaling Mechanisms. Annu. Rev. Plant Biol. 2006, 57, 837–858; https://doi.org/10.1146/annurev.arplant.56.032604.144208.Suche in Google Scholar PubMed PubMed Central
35. Losi, A. Flavin-based Blue-Light Photosensors: A Photobiophysics Update. Photochem. Photobiol. 2007, 83, 1283–1300; https://doi.org/10.1111/j.1751-1097.2007.00196.x.Suche in Google Scholar PubMed
36. Möglich, A.; Yang, X.; Ayers, R. A.; Moffat, K. Structure and Function of Plant Photoreceptors. Annu. Rev. Plant Biol. 2010, 61, 21–47; https://doi.org/10.1146/annurev-arplant-042809-112259.Suche in Google Scholar PubMed
37. Conrad, K. S.; Manahan, C. C.; Crane, B. R. Photochemistry of Flavoprotein Light Sensors. Nat. Chem. Biol. 2014, 10, 801–809; https://doi.org/10.1038/nchembio.1633.Suche in Google Scholar PubMed PubMed Central
38. Anders, K.; Essen, L.-O. The Family of Phytochrome-like Photoreceptors: Diverse, Complex and Multi-Colored, but Very Useful. Curr. Opin. Struct. Biol. 2015, 35, 7–16; https://doi.org/10.1016/j.sbi.2015.07.005.Suche in Google Scholar PubMed
39. Mouritsen, H. Long-distance Navigation and Magnetoreception in Migratory Animals. Nature 2018, 558, 50–59; https://doi.org/10.1038/s41586-018-0176-1.Suche in Google Scholar PubMed
40. Polli, D.; Rivalta, I.; Nenov, A.; Weingart, O.; Garavelli, M.; Cerullo, G. Tracking the Primary Photoconversion Events in Rhodopsins by Ultrafast Optical Spectroscopy. Photochem. Photobiol. Sci. 2014, 14, 213–228; https://doi.org/10.1039/c4pp00370e.Suche in Google Scholar PubMed
41. Renger, T.; Müh, F. Understanding Photosynthetic Light-Harvesting: a Bottom up Theoretical Approach. Phys. Chem. Chem. Phys. 2013, 15, 3348–24; https://doi.org/10.1039/c3cp43439g.Suche in Google Scholar PubMed
42. Curutchet, C.; Mennucci, B. Quantum Chemical Studies of Light Harvesting. Chem. Rev. 2017, 117, 294–343; https://doi.org/10.1021/acs.chemrev.5b00700.Suche in Google Scholar PubMed
43. Cignoni, E.; Slama, V.; Cupellini, L.; Mennucci, B. The Atomistic Modeling of Light-Harvesting Complexes from the Physical Models to the Computational Protocol. J. Chem. Phys. 2022, 156, 120901; https://doi.org/10.1063/5.0086275.Suche in Google Scholar PubMed
44. Segatta, F.; Cupellini, L.; Garavelli, M.; Mennucci, B. Quantum Chemical Modeling of the Photoinduced Activity of Multichromophoric Biosystems. Chem. Rev. 2019, 119, 9361–9380; https://doi.org/10.1021/acs.chemrev.9b00135.Suche in Google Scholar PubMed PubMed Central
45. Maity, S.; Kleinekathöfer, U. Recent Progress in Atomistic Modeling of Light-Harvesting Complexes: a Mini Review. Photosynth. Res. 2023, 156, 147–162; https://doi.org/10.1007/s11120-022-00969-w.Suche in Google Scholar PubMed PubMed Central
46. Loco, D.; Lagardère, L.; Cisneros, G. A.; Scalmani, G.; Frisch, M.; Lipparini, F.; Mennucci, B.; Piquemal, J.-P. Towards Large Scale Hybrid QM/MM Dynamics of Complex Systems with Advanced Point Dipole Polarizable Embeddings. Chem. Sci. 2019, 10, 7200–7211; https://doi.org/10.1039/c9sc01745c.Suche in Google Scholar PubMed PubMed Central
47. Nottoli, M.; Bondanza, M.; Mazzeo, P.; Cupellini, L.; Curutchet, C.; Loco, D.; Lagardère, L.; Piquemal, J.-P.; Mennucci, B.; Lipparini, F. QM/AMOEBA Description of Properties and Dynamics of Embedded Molecules. Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2023, 13; https://doi.org/10.1002/wcms.1674.Suche in Google Scholar
48. Davydov, A. S. Theory of Molecular Excitons; Plenum Press: New York, 1971.10.1007/978-1-4899-5169-4Suche in Google Scholar
49. Cupellini, L.; Corbella, M.; Mennucci, B.; Curutchet, C. Electronic Energy Transfer in Biomacromolecules. Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2019, 9, e1392; https://doi.org/10.1002/wcms.1392.Suche in Google Scholar
50. You, Z.-Q.; Hsu, C.-P. Theory and Calculation for the Electronic Coupling in Excitation Energy Transfer. Int. J. Quantum Chem. 2013, 114, 102–115; https://doi.org/10.1002/qua.24528.Suche in Google Scholar
51. Cheng, Y.-C.; Fleming, G. R. Dynamics of Light Harvesting in Photosynthesis. Annu. Rev. Phys. Chem. 2009, 60, 241–262; https://doi.org/10.1146/annurev.physchem.040808.090259.Suche in Google Scholar PubMed
52. Jang, S. J.; Mennucci, B. Delocalized Excitons in Natural Light-Harvesting Complexes. Rev. Mod. Phys. 2018, 90, 035003; https://doi.org/10.1103/revmodphys.90.035003.Suche in Google Scholar
53. 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, 224103–14; https://doi.org/10.1063/1.4769079.Suche in Google Scholar PubMed
54. Damjanović, A.; Kosztin, I.; Kleinekathöfer, U.; Schulten, K. Excitons in a Photosynthetic Light-Harvesting System: A Combined Molecular Dynamics, Quantum Chemistry, and Polaron Model Study. Phys. Rev. E 2002, 65, 031919; https://doi.org/10.1103/physreve.65.031919.Suche in Google Scholar PubMed
55. Lee, M. K.; Huo, P.; Coker, D. F. Semiclassical Path Integral Dynamics: Photosynthetic Energy Transfer with Realistic Environment Interactions. Annu. Rev. Phys. Chem. 2016, 67, 639–668; https://doi.org/10.1146/annurev-physchem-040215-112252.Suche in Google Scholar PubMed
56. Novoderezhkin, V.; Marin, A.; Grondelle, R. V. Intra-and Inter-monomeric Transfers in the Light Harvesting LHCII Complex: the Redfield–Förster Picture. Phys. Chem. Chem. Phys. 2011, 13, 17093–11.10.1039/c1cp21079cSuche in Google Scholar PubMed
57. Yang, M.; Fleming, G. R. Influence of Phonons on Exciton Transfer Dynamics: Comparison of the Redfield, Förster, and Modified Redfield Equations. Chem. Phys. 2002, 275, 355–372; https://doi.org/10.1016/s0301-0104-01-00540-7.Suche in Google Scholar
58. Scholes, G. D.; Jordanides, X. J.; Fleming, G. R. Adapting the Förster Theory of Energy Transfer for Modeling Dynamics in Aggregated Molecular Assemblies. J. Phys. Chem. B 2001, 105, 1640–1651; https://doi.org/10.1021/jp003571m.Suche in Google Scholar
59. Levine, B. G.; Martínez, T. J. Isomerization Through Conical Intersections. Annu. Rev. Phys. Chem. 2007, 58, 613–634; https://doi.org/10.1146/annurev.physchem.57.032905.104612.Suche in Google Scholar PubMed
60. Polli, D.; Altoè, P.; Weingart, O.; Spillane, K. M.; Manzoni, C.; Brida, D.; Tomasello, G.; Orlandi, G.; Kukura, P.; Mathies, R. A.; Garavelli, M.; Cerullo, G. Conical Intersection Dynamics of the Primary Photoisomerization Event in Vision. Nature 2010, 467, 440–443; https://doi.org/10.1038/nature09346.Suche in Google Scholar PubMed
61. Gozem, S.; Luk, H. L.; Schapiro, I.; Olivucci, M. Theory and Simulation of the Ultrafast Double-Bond Isomerization of Biological Chromophores. Chem. Rev. 2017, 117, 13502–13565; https://doi.org/10.1021/acs.chemrev.7b00177.Suche in Google Scholar PubMed
62. Sen, S.; Kar, R. K.; Borin, V. A.; Schapiro, I. Insight into the Isomerization Mechanism of Retinal Proteins from Hybrid Quantum Mechanics/molecular Mechanics Simulations. WIREs Comput. Mol. Sci. 2022, 12, e1562; https://doi.org/10.1002/wcms.1562.Suche in Google Scholar
63. Frutos, L. M.; Andruniów, T.; Santoro, F.; Ferré, N.; Olivucci, M. Tracking the Excited-State Time Evolution of the Visual Pigment with Multiconfigurational Quantum Chemistry, Proc. Natl. Acad. Sci. 2007, 104, 7764–7769; https://doi.org/10.1073/pnas.0701732104.Suche in Google Scholar PubMed PubMed Central
64. 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, 1526–28; https://doi.org/10.1007/s00214-014-1526-1.Suche in Google Scholar
65. Crespo-Otero, R.; Barbatti, M. Recent Advances and Perspectives on Nonadiabatic Mixed Quantum–Classical Dynamics. Chem. Rev. 2018, 118, 7026–7068; https://doi.org/10.1021/acs.chemrev.7b00577.Suche in Google Scholar PubMed
66. Nelson, T. R.; White, A. J.; Bjorgaard, J. A.; Sifain, A. E.; Zhang, Y.; Nebgen, B.; Fernandez-Alberti, S.; Mozyrsky, D.; Roitberg, A. E.; Tretiak, S. Non-adiabatic Excited-State Molecular Dynamics: Theory and Applications for Modeling Photophysics in Extended Molecular Materials. Chem. Rev. 2020, 120, 2215–2287; https://doi.org/10.1021/acs.chemrev.9b00447.Suche in Google Scholar PubMed
67. Mai, S.; González, L. Molecular Photochemistry: Recent Developments in Theory. Angew. Chem., Int. Ed. 2020, 59, 16832–16846; https://doi.org/10.1002/anie.201916381.Suche in Google Scholar PubMed PubMed Central
68. Tully, J. C. Molecular Dynamics with Electronic Transitions. J. Chem. Phys. 1990, 93, 1061–1071; https://doi.org/10.1063/1.459170.Suche in Google Scholar
69. Yang, X.; Manathunga, M.; Gozem, S.; Léonard, J.; Andruniów, T.; Olivucci, M. Quantum–Classical Simulations of Rhodopsin Reveal Excited-State Population Splitting and its Effects on Quantum Efficiency. Nat. Chem. 2022, 14, 441–449; https://doi.org/10.1038/s41557-022-00892-6.Suche in Google Scholar PubMed PubMed Central
70. Chung, W. C.; Nanbu, S.; Ishida, T. QM/MM Trajectory Surface Hopping Approach to Photoisomerization of Rhodopsin and Isorhodopsin: The Origin of Faster and More Efficient Isomerization for Rhodopsin. J. Phys. Chem. B 2012, 116, 8009–8023; https://doi.org/10.1021/jp212378u.Suche in Google Scholar PubMed
71. Salvadori, G.; Macaluso, V.; Pellicci, G.; Cupellini, L.; Granucci, G.; Mennucci, B. Protein Control of Photochemistry and Transient Intermediates in Phytochromes. Nat. Commun. 2022, 13, 6838; https://doi.org/10.1038/s41467-022-34640-8.Suche in Google Scholar PubMed PubMed Central
72. Morozov, D.; Modi, V.; Mironov, V.; Groenhof, G. The Photocycle of Bacteriophytochrome Is Initiated by Counterclockwise Chromophore Isomerization. J. Phys. Chem. Lett. 2022, 13, 4538–4542; https://doi.org/10.1021/acs.jpclett.2c00899.Suche in Google Scholar PubMed PubMed Central
73. Curchod, B. F. E.; Martínez, T. J. Ab Initio Nonadiabatic Quantum Molecular Dynamics. Chem. Rev. 2018, 118, 3305–3336; https://doi.org/10.1021/acs.chemrev.7b00423.Suche in Google Scholar PubMed
74. Thiel, W. Semiempirical Quantum-Chemical Methods. Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2013, 4, 145–157; https://doi.org/10.1002/wcms.1161.Suche in Google Scholar
75. Fabiano, E.; Keal, T. W.; Thiel, W. Implementation of Surface Hopping Molecular Dynamics Using Semiempirical Methods. Chem. Phys. 2008, 349, 334–347; https://doi.org/10.1016/j.chemphys.2008.01.044.Suche in Google Scholar
76. Rosso, K. M.; Dupuis, M. Electron Transfer in Environmental Systems: A Frontier for Theoretical Chemistry. Theor. Chem. Acc. 2006, 116, 124–136; https://doi.org/10.1007/s00214-005-0016-x.Suche in Google Scholar
77. Beratan, D. N.; Liu, C.; Migliore, A.; Polizzi, N. F.; Skourtis, S. S.; Zhang, P.; Zhang, Y. Charge Transfer in Dynamical Biosystems, or the Treachery of (Static) Images. Acc. Chem. Res. 2015, 48, 474–481; https://doi.org/10.1021/ar500271d.Suche in Google Scholar PubMed PubMed Central
78. Blumberger, J. Recent Advances in the Theory and Molecular Simulation of Biological Electron Transfer Reactions. Chem. Rev. 2015, 115, 11191–11238; https://doi.org/10.1021/acs.chemrev.5b00298.Suche in Google Scholar PubMed
79. Narth, C.; Gillet, N.; Cailliez, F.; Lévy, B.; de la Lande, A. Electron Transfer, Decoherence, and Protein Dynamics: Insights from Atomistic Simulations. Acc. Chem. Res. 2015, 48, 1090–1097; https://doi.org/10.1021/ar5002796.Suche in Google Scholar PubMed
80. Escudero, D. Revising Intramolecular Photoinduced Electron Transfer (PET) from First-Principles. Acc. Chem. Res. 2016, 49, 1816–1824; https://doi.org/10.1021/acs.accounts.6b00299.Suche in Google Scholar PubMed
81. Saen-Oon, S.; Lucas, M. F.; Guallar, V. Electron Transfer in Proteins: Theory, Applications and Future Perspectives. Phys. Chem. Chem. Phys. 2013, 15, 15271–15285; https://doi.org/10.1039/c3cp50484k.Suche in Google Scholar PubMed
82. Hammes-Schiffer, S. Exploring Proton-Coupled Electron Transfer at Multiple Scales. Nat. Comput. Sci. 2023, 3, 291–300; https://doi.org/10.1038/s43588-023-00422-5.Suche in Google Scholar PubMed PubMed Central
83. Zanetti‐Polzi, L.; Pantazis, D. A.; Daidone, I. Intermolecular Photoinduced Electron Transfer in Biosystems: Impact of Conformational Transitions and Multiple Channels on Kinetics. ChemPhotoChem 2024, 8, e202300307; https://doi.org/10.1002/cptc.202300307.Suche in Google Scholar
84. Marcus, R. A. Chemical and Electrochemical Electron-Transfer Theory. Annu. Rev. Phys. Chem. 1964, 15, 155–196; https://doi.org/10.1146/annurev.pc.15.100164.001103.Suche in Google Scholar
85. Oberhofer, H.; Reuter, K.; Blumberger, J. Charge Transport in Molecular Materials: An Assessment of Computational Methods. Chem. Rev. 2017, 117, 10319–10357; https://doi.org/10.1021/acs.chemrev.7b00086.Suche in Google Scholar PubMed
86. Dral, P. O.; Barbatti, M.; Thiel, W. Nonadiabatic Excited-State Dynamics with Machine Learning. J. Phys. Chem. Lett. 2018, 9, 5660–5663; https://doi.org/10.1021/acs.jpclett.8b02469.Suche in Google Scholar PubMed PubMed Central
87. Dral, P. O. Quantum Chemistry in the Age of Machine Learning. J. Phys. Chem. Lett. 2020, 11, 2336–2347; https://doi.org/10.1021/acs.jpclett.9b03664.Suche in Google Scholar PubMed
88. Westermayr, J.; Marquetand, P. Machine Learning for Electronically Excited States of Molecules. Chem. Rev. 2021, 121, 9873–9926; https://doi.org/10.1021/acs.chemrev.0c00749.Suche in Google Scholar PubMed PubMed Central
89. Richings, G. W.; Habershon, S. Predicting Molecular Photochemistry Using Machine-Learning-Enhanced Quantum Dynamics Simulations. Acc. Chem. Res. 2022, 55, 209–220; https://doi.org/10.1021/acs.accounts.1c00665.Suche in Google Scholar PubMed
90. Häse, F.; Valleau, S.; Pyzer-Knapp, E.; Aspuru-Guzik, A. Machine Learning Exciton Dynamics. Chem. Sci. 2016, 7, 5139–5147; https://doi.org/10.1039/c5sc04786b.Suche in Google Scholar PubMed PubMed Central
91. Sokolov, M.; Hoffmann, D. S.; Dohmen, P. M.; Krämer, M.; Höfener, S.; Kleinekathöfer, U.; Elstner, M. Non-Adiabatic Molecular Dynamics Simulations Provide New Insights into the Exciton Transfer in the Fenna–Matthews–Olson Complex. Phys. Chem. Chem. Phys. 2024, 26, 19469–19496; https://doi.org/10.1039/d4cp02116a.Suche in Google Scholar PubMed
92. Cignoni, E.; Cupellini, L.; Mennucci, B. Machine Learning Exciton Hamiltonians in Light-Harvesting Complexes. J. Chem. Theory Comput. 2023, 19, 965–977; https://doi.org/10.1021/acs.jctc.2c01044.Suche in Google Scholar PubMed PubMed Central
© 2025 IUPAC & De Gruyter
