The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter
Abstract Challenging the basis of our chemical intuition, recent experimental evidence reveals the presence of a new type of intrinsic fluorescence in biomolecules that exists even in the absence of aromatic or electronically conjugated chemical compounds. The origin of this phenomenon has remained...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-42874-3 |
| _version_ | 1797558223989899264 |
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| author | Gonzalo Díaz Mirón Jonathan A. Semelak Luca Grisanti Alex Rodriguez Irene Conti Martina Stella Jayaramakrishnan Velusamy Nicola Seriani Nadja Došlić Ivan Rivalta Marco Garavelli Dario A. Estrin Gabriele S. Kaminski Schierle Mariano C. González Lebrero Ali Hassanali Uriel N. Morzan |
| author_facet | Gonzalo Díaz Mirón Jonathan A. Semelak Luca Grisanti Alex Rodriguez Irene Conti Martina Stella Jayaramakrishnan Velusamy Nicola Seriani Nadja Došlić Ivan Rivalta Marco Garavelli Dario A. Estrin Gabriele S. Kaminski Schierle Mariano C. González Lebrero Ali Hassanali Uriel N. Morzan |
| author_sort | Gonzalo Díaz Mirón |
| collection | DOAJ |
| description | Abstract Challenging the basis of our chemical intuition, recent experimental evidence reveals the presence of a new type of intrinsic fluorescence in biomolecules that exists even in the absence of aromatic or electronically conjugated chemical compounds. The origin of this phenomenon has remained elusive so far. In the present study, we identify a mechanism underlying this new type of fluorescence in different biological aggregates. By employing non-adiabatic ab initio molecular dynamics simulations combined with a data-driven approach, we characterize the typical ultrafast non-radiative relaxation pathways active in non-fluorescent peptides. We show that the key vibrational mode for the non-radiative decay towards the ground state is the carbonyl elongation. Non-aromatic fluorescence appears to emerge from blocking this mode with strong local interactions such as hydrogen bonds. While we cannot rule out the existence of alternative non-aromatic fluorescence mechanisms in other systems, we demonstrate that this carbonyl-lock mechanism for trapping the excited state leads to the fluorescence yield increase observed experimentally, and set the stage for design principles to realize novel non-invasive biocompatible probes with applications in bioimaging, sensing, and biophotonics. |
| first_indexed | 2024-03-10T17:28:18Z |
| format | Article |
| id | doaj.art-4bd339f5319f46e9b865bb05545ddf7c |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:28:18Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-4bd339f5319f46e9b865bb05545ddf7c2023-11-20T10:06:48ZengNature PortfolioNature Communications2041-17232023-11-0114111310.1038/s41467-023-42874-3The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matterGonzalo Díaz Mirón0Jonathan A. Semelak1Luca Grisanti2Alex Rodriguez3Irene Conti4Martina Stella5Jayaramakrishnan Velusamy6Nicola Seriani7Nadja Došlić8Ivan Rivalta9Marco Garavelli10Dario A. Estrin11Gabriele S. Kaminski Schierle12Mariano C. González Lebrero13Ali Hassanali14Uriel N. Morzan15Departamento de Química Inorgánica, Analítica y Química Física, Instituto de Química Física de los Materiales, Medio Ambiente y Energía (INQUIMAE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos AiresDepartamento de Química Inorgánica, Analítica y Química Física, Instituto de Química Física de los Materiales, Medio Ambiente y Energía (INQUIMAE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos AiresDivision of Theoretical Physics, Ruder Bošković InstituteCondensed Matter and Statistical Physics, The Abdus Salam International Centre for Theoretical PhysicsDipartimento di Chimica industriale “Toso Montanari”, Università di BolognaCondensed Matter and Statistical Physics, The Abdus Salam International Centre for Theoretical PhysicsChemical Engineering and Biotechnology, University of CambridgeCondensed Matter and Statistical Physics, The Abdus Salam International Centre for Theoretical PhysicsDivision of Theoretical Physics, Ruder Bošković InstituteDipartimento di Chimica industriale “Toso Montanari”, Università di BolognaDipartimento di Chimica industriale “Toso Montanari”, Università di BolognaDepartamento de Química Inorgánica, Analítica y Química Física, Instituto de Química Física de los Materiales, Medio Ambiente y Energía (INQUIMAE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos AiresChemical Engineering and Biotechnology, University of CambridgeDepartamento de Química Inorgánica, Analítica y Química Física, Instituto de Química Física de los Materiales, Medio Ambiente y Energía (INQUIMAE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos AiresCondensed Matter and Statistical Physics, The Abdus Salam International Centre for Theoretical PhysicsCondensed Matter and Statistical Physics, The Abdus Salam International Centre for Theoretical PhysicsAbstract Challenging the basis of our chemical intuition, recent experimental evidence reveals the presence of a new type of intrinsic fluorescence in biomolecules that exists even in the absence of aromatic or electronically conjugated chemical compounds. The origin of this phenomenon has remained elusive so far. In the present study, we identify a mechanism underlying this new type of fluorescence in different biological aggregates. By employing non-adiabatic ab initio molecular dynamics simulations combined with a data-driven approach, we characterize the typical ultrafast non-radiative relaxation pathways active in non-fluorescent peptides. We show that the key vibrational mode for the non-radiative decay towards the ground state is the carbonyl elongation. Non-aromatic fluorescence appears to emerge from blocking this mode with strong local interactions such as hydrogen bonds. While we cannot rule out the existence of alternative non-aromatic fluorescence mechanisms in other systems, we demonstrate that this carbonyl-lock mechanism for trapping the excited state leads to the fluorescence yield increase observed experimentally, and set the stage for design principles to realize novel non-invasive biocompatible probes with applications in bioimaging, sensing, and biophotonics.https://doi.org/10.1038/s41467-023-42874-3 |
| spellingShingle | Gonzalo Díaz Mirón Jonathan A. Semelak Luca Grisanti Alex Rodriguez Irene Conti Martina Stella Jayaramakrishnan Velusamy Nicola Seriani Nadja Došlić Ivan Rivalta Marco Garavelli Dario A. Estrin Gabriele S. Kaminski Schierle Mariano C. González Lebrero Ali Hassanali Uriel N. Morzan The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter Nature Communications |
| title | The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter |
| title_full | The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter |
| title_fullStr | The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter |
| title_full_unstemmed | The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter |
| title_short | The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter |
| title_sort | carbonyl lock mechanism underlying non aromatic fluorescence in biological matter |
| url | https://doi.org/10.1038/s41467-023-42874-3 |
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