Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine

Julia Dietler; Renate Gelfert; Jennifer Kaiser; Veniamin Borin; Christian Renzl; Sebastian Pilsl; Américo Tavares Ranzani; Andrés García de Fuentes; Tobias Gleichmann; Ralph P. Diensthuber; Michael Weyand; Günter Mayer; Igor Schapiro; Andreas Möglich

doi:10.1038/s41467-022-30252-4

Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine

Julia Dietler, Renate Gelfert, Jennifer Kaiser, Veniamin Borin, Christian Renzl, Sebastian Pilsl, Américo Tavares Ranzani, Andrés García de Fuentes, Tobias Gleichmann, Ralph P. Diensthuber, Michael Weyand, Günter Mayer, Igor Schapiro, Andreas Möglich^*

^*Corresponding author for this work

Institute of Chemistry

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

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.

Original language	American English
Article number	2618
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-30252-4
State	Published - 12 May 2022

Bibliographical note

Funding 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.

Funding Information:
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.

Publisher Copyright:
© 2022, The Author(s).

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Dietler, J., Gelfert, R., Kaiser, J., Borin, V., Renzl, C., Pilsl, S., Ranzani, A. T., García de Fuentes, A., Gleichmann, T., Diensthuber, R. P., Weyand, M., Mayer, G., Schapiro, I., & Möglich, A. (2022). Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine. Nature Communications, 13(1), Article 2618. https://doi.org/10.1038/s41467-022-30252-4

@article{2a6e94df86c243dfb7dd606a03f56321,

title = "Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine",

abstract = "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 {\AA} 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.",

author = "Julia Dietler and Renate Gelfert and Jennifer Kaiser and Veniamin Borin and Christian Renzl and Sebastian Pilsl and Ranzani, {Am{\'e}rico Tavares} and {Garc{\'i}a de Fuentes}, Andr{\'e}s and Tobias Gleichmann and Diensthuber, {Ralph P.} and Michael Weyand and G{\"u}nter Mayer and Igor Schapiro and Andreas M{\"o}glich",

note = "Funding 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. Funding Information: 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. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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doi = "10.1038/s41467-022-30252-4",

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T1 - Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine

AU - Dietler, Julia

AU - Gelfert, Renate

AU - Kaiser, Jennifer

AU - Borin, Veniamin

AU - Renzl, Christian

AU - Pilsl, Sebastian

AU - Ranzani, Américo Tavares

AU - García de Fuentes, Andrés

AU - Gleichmann, Tobias

AU - Diensthuber, Ralph P.

AU - Weyand, Michael

AU - Mayer, Günter

AU - Schapiro, Igor

AU - Möglich, Andreas

N1 - Funding 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. Funding Information: 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. Publisher Copyright: © 2022, The Author(s).

PY - 2022/5/12

Y1 - 2022/5/12

N2 - 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.

AB - 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.

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AN - SCOPUS:85130041158

SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2618

ER -

Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine

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