CryoRhodopsins: a comprehensive characterization of a group of microbial rhodopsins from cold environments

Author:

Lamm G.H.U.ORCID,Marin E.ORCID,Alekseev A.ORCID,Schellbach A.V.,Stetsenko A.ORCID,Bourenkov G.ORCID,Borshchevskiy V.ORCID,Asido M.ORCID,Agthe M.ORCID,Engilberge S.ORCID,Rose S.L.ORCID,Caramello N.ORCID,Royant A.ORCID,Schneider T. R.,Bateman A.ORCID,Mager T.ORCID,Moser T.ORCID,Wachtveitl J.ORCID,Guskov A.ORCID,Kovalev K.ORCID

Abstract

ABSTRACTMicrobial rhodopsins are omnipresent on Earth, however the vast majority of them remain uncharacterized. Here we describe a new rhodopsin group from cold-adapted organisms and cold environments, such as glaciers, denoted as CryoRhodopsins (CryoRs). Our data suggest that CryoRs have dual functionality switching between inward transmembrane proton translocation and photosensory activity, both of which can be modulated with UV light. CryoR1 exhibits two subpopulations in the ground state, which upon light activation lead to transient photocurrents of opposing polarities. A distinguishing feature of the group is the presence of a buried arginine residue close to the cytoplasmic face of its members. Combining single-particle cryo-electron microscopy and X-ray crystallography with the rhodopsin activation by light, we demonstrate that the arginine stabilizes a UV-absorbing intermediate of an extremely slow CryoRhodopsin photocycle. Together with extensive spectroscopic characterization, our investigations on CryoR1 and CryoR2 proteins reveal mechanisms of photoswitching in the newly identified group and demonstrate principles of the adaptation of these rhodopsins to low temperatures.

Publisher

Cold Spring Harbor Laboratory

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