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Sci Adv. 2017 Sep 22;3(9):e1603187. doi: 10.1126/sciadv.1603187. eCollection 2017 Sep.

Inward H+ pump xenorhodopsin: Mechanism and alternative optogenetic approach.

Author information

1
Institute of Complex Systems (ICS), ICS-6: Structural Biochemistry, Research Centre Jülich, Jülich, Germany.
2
Institute of Crystallography, RWTH Aachen University, Aachen, Germany.
3
Moscow Institute of Physics and Technology, Dolgoprudny, Russia.
4
Max Planck Institute of Biophysics, Frankfurt am Main, Germany.
5
Institut de Biologie Structurale Jean-Pierre Ebel, Université Grenoble Alpes-Commissariat à l'Energie Atomique et aux Energies Alternatives-CNRS, Grenoble, France.
6
Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland.
7
Institute for Biophysical Chemistry, Hannover Medical School, Hannover, Germany.
8
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands.
9
Institute of Hydrobiology, Department of Aquatic Microbial Ecology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic.
10
Joint Institute for Nuclear Research, Dubna, Russia.
11
European Synchrotron Radiation Facility, 38027 Grenoble, France.
12
Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández, San Juan de Alicante, Alicante, Spain.
13
Division for Structural Biochemistry, Hannover Medical School, Hannover, Germany.

Abstract

Generation of an electrochemical proton gradient is the first step of cell bioenergetics. In prokaryotes, the gradient is created by outward membrane protein proton pumps. Inward plasma membrane native proton pumps are yet unknown. We describe comprehensive functional studies of the representatives of the yet noncharacterized xenorhodopsins from Nanohaloarchaea family of microbial rhodopsins. They are inward proton pumps as we demonstrate in model membrane systems, Escherichia coli cells, human embryonic kidney cells, neuroblastoma cells, and rat hippocampal neuronal cells. We also solved the structure of a xenorhodopsin from the nanohalosarchaeon Nanosalina (NsXeR) and suggest a mechanism of inward proton pumping. We demonstrate that the NsXeR is a powerful pump, which is able to elicit action potentials in rat hippocampal neuronal cells up to their maximal intrinsic firing frequency. Hence, inwardly directed proton pumps are suitable for light-induced remote control of neurons, and they are an alternative to the well-known cation-selective channelrhodopsins.

PMID:
28948217
PMCID:
PMC5609834
DOI:
10.1126/sciadv.1603187
[Indexed for MEDLINE]
Free PMC Article

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