Retinal chromophore charge delocalization and confinement explain the extreme photophysics of Neorhodopsin

Riccardo Palombo; Leonardo Barneschi; Laura Pedraza-González; Daniele Padula; Igor Schapiro; Massimo Olivucci

doi:10.1038/s41467-022-33953-y

Retinal chromophore charge delocalization and confinement explain the extreme photophysics of Neorhodopsin

Riccardo Palombo, Leonardo Barneschi, Laura Pedraza-González, Daniele Padula, Igor Schapiro, Massimo Olivucci^*

^*Corresponding author for this work

Institute of Chemistry

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

The understanding of how the rhodopsin sequence can be modified to exactly modulate the spectroscopic properties of its retinal chromophore, is a prerequisite for the rational design of more effective optogenetic tools. One key problem is that of establishing the rules to be satisfied for achieving highly fluorescent rhodopsins with a near infrared absorption. In the present paper we use multi-configurational quantum chemistry to construct a computer model of a recently discovered natural rhodopsin, Neorhodopsin, displaying exactly such properties. We show that the model, that successfully replicates the relevant experimental observables, unveils a geometrical and electronic structure of the chromophore featuring a highly diffuse charge distribution along its conjugated chain. The same model reveals that a charge confinement process occurring along the chromophore excited state isomerization coordinate, is the primary cause of the observed fluorescence enhancement.

Original language	American English
Article number	6652
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-33953-y
State	Published - Dec 2022

Bibliographical note

Funding Information:
The research has been in part supported by Grants NSF CHE-CLP-1710191 and NIH GM126627-01. The authors are also grateful for a Department of Excellence Grant 2018-2022 funded by the Italian MIUR and by Fondazione Banca d’Italia for providing equipment funds. D.P. acknowledges the Italian Ministry of University and Research (MUR) for a Rita Levi Montalcini grant. We thank Suliman Adam for having provided the NeoR homology model used in this work. I.S. acknowledges support by the DFG through SFB 1078, project C6. I.S. thanks the Israel Science Foundation (Research Center grant no. 3131/20). L.B. and M.O. acknowledge partial support from European Union, Next Generation EU, MUR Italia Domani Progetto mRNA Spoke 6 del “National Center for Gene Therapy and Drugs based on RNA Technology”, CUP di progetto B63C22000610006.

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© 2022, The Author(s).

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title = "Retinal chromophore charge delocalization and confinement explain the extreme photophysics of Neorhodopsin",

abstract = "The understanding of how the rhodopsin sequence can be modified to exactly modulate the spectroscopic properties of its retinal chromophore, is a prerequisite for the rational design of more effective optogenetic tools. One key problem is that of establishing the rules to be satisfied for achieving highly fluorescent rhodopsins with a near infrared absorption. In the present paper we use multi-configurational quantum chemistry to construct a computer model of a recently discovered natural rhodopsin, Neorhodopsin, displaying exactly such properties. We show that the model, that successfully replicates the relevant experimental observables, unveils a geometrical and electronic structure of the chromophore featuring a highly diffuse charge distribution along its conjugated chain. The same model reveals that a charge confinement process occurring along the chromophore excited state isomerization coordinate, is the primary cause of the observed fluorescence enhancement.",

author = "Riccardo Palombo and Leonardo Barneschi and Laura Pedraza-Gonz{\'a}lez and Daniele Padula and Igor Schapiro and Massimo Olivucci",

note = "Funding Information: The research has been in part supported by Grants NSF CHE-CLP-1710191 and NIH GM126627-01. The authors are also grateful for a Department of Excellence Grant 2018-2022 funded by the Italian MIUR and by Fondazione Banca d{\textquoteright}Italia for providing equipment funds. D.P. acknowledges the Italian Ministry of University and Research (MUR) for a Rita Levi Montalcini grant. We thank Suliman Adam for having provided the NeoR homology model used in this work. I.S. acknowledges support by the DFG through SFB 1078, project C6. I.S. thanks the Israel Science Foundation (Research Center grant no. 3131/20). L.B. and M.O. acknowledge partial support from European Union, Next Generation EU, MUR Italia Domani Progetto mRNA Spoke 6 del “National Center for Gene Therapy and Drugs based on RNA Technology”, CUP di progetto B63C22000610006. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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AU - Schapiro, Igor

AU - Olivucci, Massimo

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AB - The understanding of how the rhodopsin sequence can be modified to exactly modulate the spectroscopic properties of its retinal chromophore, is a prerequisite for the rational design of more effective optogenetic tools. One key problem is that of establishing the rules to be satisfied for achieving highly fluorescent rhodopsins with a near infrared absorption. In the present paper we use multi-configurational quantum chemistry to construct a computer model of a recently discovered natural rhodopsin, Neorhodopsin, displaying exactly such properties. We show that the model, that successfully replicates the relevant experimental observables, unveils a geometrical and electronic structure of the chromophore featuring a highly diffuse charge distribution along its conjugated chain. The same model reveals that a charge confinement process occurring along the chromophore excited state isomerization coordinate, is the primary cause of the observed fluorescence enhancement.

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Retinal chromophore charge delocalization and confinement explain the extreme photophysics of Neorhodopsin

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