QuasAr Odyssey: the origin of fluorescence and its voltage sensitivity in microbial rhodopsins

Arita Silapetere (), Songhwan Hwang, Yusaku Hontani, Rodrigo G. Fernandez Lahore, Jens Balke, Francisco Velazquez Escobar, Martijn Tros, Patrick E. Konold, Rainer Matis, Roberta Croce, Peter J. Walla, Peter Hildebrandt, Ulrike Alexiev, John T. M. Kennis, Han Sun, Tillmann Utesch () and Peter Hegemann
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Arita Silapetere: Humboldt-Universität zu Berlin
Songhwan Hwang: Humboldt-Universität zu Berlin
Yusaku Hontani: Vrije Universiteit Amsterdam
Rodrigo G. Fernandez Lahore: Humboldt-Universität zu Berlin
Jens Balke: Freie Universität Berlin
Francisco Velazquez Escobar: Technische Universität Berlin
Martijn Tros: Vrije Universiteit Amsterdam
Patrick E. Konold: Vrije Universiteit Amsterdam
Rainer Matis: Technische Universität Braunschweig
Roberta Croce: Vrije Universiteit Amsterdam
Peter J. Walla: Technische Universität Braunschweig
Peter Hildebrandt: Technische Universität Berlin
Ulrike Alexiev: Freie Universität Berlin
John T. M. Kennis: Vrije Universiteit Amsterdam
Han Sun: Leibniz-Institut für Molekulare Pharmakologie
Tillmann Utesch: Leibniz-Institut für Molekulare Pharmakologie
Peter Hegemann: Humboldt-Universität zu Berlin

Nature Communications, 2022, vol. 13, issue 1, 1-20

Abstract: Abstract Rhodopsins had long been considered non-fluorescent until a peculiar voltage-sensitive fluorescence was reported for archaerhodopsin-3 (Arch3) derivatives. These proteins named QuasArs have been used for imaging membrane voltage changes in cell cultures and small animals. However due to the low fluorescence intensity, these constructs require use of much higher light intensity than other optogenetic tools. To develop the next generation of sensors, it is indispensable to first understand the molecular basis of the fluorescence and its modulation by the membrane voltage. Based on spectroscopic studies of fluorescent Arch3 derivatives, we propose a unique photo-reaction scheme with extended excited-state lifetimes and inefficient photoisomerization. Molecular dynamics simulations of Arch3, of the Arch3 fluorescent derivative Archon1, and of several its mutants have revealed different voltage-dependent changes of the hydrogen-bonding networks including the protonated retinal Schiff-base and adjacent residues. Experimental observations suggest that under negative voltage, these changes modulate retinal Schiff base deprotonation and promote a decrease in the populations of fluorescent species. Finally, we identified molecular constraints that further improve fluorescence quantum yield and voltage sensitivity.

Date: 2022
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DOI: 10.1038/s41467-022-33084-4

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