MerMAIDs: a family of metagenomically discovered marine anion-conducting and intensely desensitizing channelrhodopsins

Johannes Oppermann, Paul Fischer, Arita Silapetere, Bernhard Liepe, Silvia Rodriguez-Rozada, José Flores-Uribe, Enrico Schiewer, Anke Keidel, Johannes Vierock, Joel Kaufmann, Matthias Broser, Meike Luck, Franz Bartl, Peter Hildebrandt, J. Simon Wiegert, Oded Béjà, Peter Hegemann () and Jonas Wietek ()
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Johannes Oppermann: Humboldt-Universität zu Berlin
Paul Fischer: Humboldt-Universität zu Berlin
Arita Silapetere: Humboldt-Universität zu Berlin
Bernhard Liepe: Humboldt-Universität zu Berlin
Silvia Rodriguez-Rozada: Center for Molecular Neurobiology Hamburg
José Flores-Uribe: Technion—Israel Institute of Technology
Enrico Schiewer: Humboldt-Universität zu Berlin
Anke Keidel: Technische Universität Berlin
Johannes Vierock: Humboldt-Universität zu Berlin
Joel Kaufmann: Humboldt-Universität zu Berlin
Matthias Broser: Humboldt-Universität zu Berlin
Meike Luck: Humboldt-Universität zu Berlin
Franz Bartl: Humboldt-Universität zu Berlin
Peter Hildebrandt: Technische Universität Berlin
J. Simon Wiegert: Center for Molecular Neurobiology Hamburg
Oded Béjà: Technion—Israel Institute of Technology
Peter Hegemann: Humboldt-Universität zu Berlin
Jonas Wietek: Humboldt-Universität zu Berlin

Nature Communications, 2019, vol. 10, issue 1, 1-13

Abstract: Abstract Channelrhodopsins (ChRs) are algal light-gated ion channels widely used as optogenetic tools for manipulating neuronal activity. ChRs desensitize under continuous bright-light illumination, resulting in a significant decline of photocurrents. Here we describe a metagenomically identified family of phylogenetically distinct anion-conducting ChRs (designated MerMAIDs). MerMAIDs almost completely desensitize during continuous illumination due to accumulation of a late non-conducting photointermediate that disrupts the ion permeation pathway. MerMAID desensitization can be fully explained by a single photocycle in which a long-lived desensitized state follows the short-lived conducting state. A conserved cysteine is the critical factor in desensitization, as its mutation results in recovery of large stationary photocurrents. The rapid desensitization of MerMAIDs enables their use as optogenetic silencers for transient suppression of individual action potentials without affecting subsequent spiking during continuous illumination. Our results could facilitate the development of optogenetic tools from metagenomic databases and enhance general understanding of ChR function.

Date: 2019
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DOI: 10.1038/s41467-019-11322-6

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