In nature as in biotechnology, light-oxygen-voltage photoreceptors perceive blue light to elicit spatiotemporally defined cellular responses. Photon absorption drives thioadduct formation between a conserved cysteine and the flavin chromophore. An equally conserved, proximal glutamine processes the resultant flavin protonation into downstream hydrogen-bond rearrangements. Here, we report that this glutamine, long deemed essential, is generally dispensable. In its absence, several light-oxygen-voltage receptors invariably retained productive, if often attenuated, signaling responses. Structures of a light-oxygen-voltage paradigm at around 1 Å resolution revealed highly similar light-induced conformational changes, irrespective of whether the glutamine is present. Naturally occurring, glutamine-deficient light-oxygen-voltage receptors likely serve as bona fide photoreceptors, as we showcase for a diguanylate cyclase. We propose that without the glutamine, water molecules transiently approach the chromophore and thus propagate flavin protonation downstream. Signaling without glutamine appears intrinsic to light-oxygen-voltage receptors, which pertains to biotechnological applications and suggests evolutionary descendance from redox-active flavoproteins.
Bibliographical noteFunding Information:
Funding by the Deutsche Forschungsgemeinschaft (DFG) (491183248; grants MO2192/6-1/2 and MO2192/8-1 to A.M.; grants MA3442/5-1/2 to G.M.) and the Alexander-von-Humboldt Foundation (Sofja-Kovalevskaya Award to A.M.) is gratefully acknowledged. I.S. acknowledges support by the DFG through SFB 1078, project C6. Open Access funding enabled and organized by Projekt DEAL, and supported by the DFG and the Open Access Publishing Fund of the University of Bayreuth.
We thank U. Jenal and B. Zoltowski for discussion; R. Hengge for discussion and supplying the E. coli reporter strain harboring the genomic csgB::lacZ integration; and C. Xu for assistance with ChemDraw. Diffraction data were collected on BL14.1 and BL14.2 at the BESSY II electron storage ring operated by the Helmholtz-Zentrum Berlin79, with the assistance of C. Feiler and F. Lennartz.
© 2022, The Author(s).