RubyACRs, nonalgal anion channelrhodopsins with highly red-shifted absorption

Channelrhodopsins are light-gated ion channels widely used to control neuronal firing with light (optogenetics). We report two previously unknown families of anion channelrhodopsins (ACRs), one from the heterotrophic protists labyrinthulea and the other from haptophyte algae. Four closely related la...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2020-09, Vol.117 (37), p.22833-22840
Main Authors: Govorunova, Elena G., Sineshchekov, Oleg A., Li, Hai, Wang, Yumei, Brown, Leonid S., Spudich, John L.
Format: Article
Language:English
Subjects:
Absorption
Algae
Anions
Anions - metabolism
Biological Sciences
Channel gating
Channelrhodopsins - chemistry
Chromophores
Color sensitivity
Color vision
Cryptophyta - genetics
Decay rate
Energy transfer
Fluorescence
Genetics
HEK293 Cells
Humans
Information processing
Ion Channel Gating - physiology
Ion channels
Ion Channels - chemistry
Ion Channels - metabolism
Light
Membrane Potentials - physiology
Microorganisms
Neurons - metabolism
Optics
Optogenetics - methods
Photoelectric effect
Photoelectric emission
Retina
Rhodopsin - metabolism
Spectra
Spectral sensitivity
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Summary:Channelrhodopsins are light-gated ion channels widely used to control neuronal firing with light (optogenetics). We report two previously unknown families of anion channelrhodopsins (ACRs), one from the heterotrophic protists labyrinthulea and the other from haptophyte algae. Four closely related labyrinthulea ACRs, named RubyACRs here, exhibit a unique retinal-binding pocket that creates spectral sensitivities with maxima at 590 to 610 nm, the most red-shifted channelrhodopsins known, long-sought for optogenetics, and more broadly the most red-shifted microbial rhodopsins thus far reported. We identified three spectral tuning residues critical for the red-shifted absorption. Photocurrents recorded from the RubyACR from Aurantiochytrium limacinum (designated AlACR1) under single-turnover excitation exhibited biphasic decay, the rate of which was only weakly voltage dependent, in contrast to that in previously characterized cryptophyte ACRs, indicating differences in channel gating mechanisms between the two ACR families. Moreover, in A. limacinum we identified three ACRs with absorption maxima at 485, 545, and 590 nm, indicating color-sensitive photosensing with blue, green, and red spectral variation of ACRs within individual species of the labyrinthulea family. We also report functional energy transfer from a cytoplasmic fluorescent protein domain to the retinal chromophore bound within RubyACRs.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2005981117