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

Author

Listed:
  • Julia Dietler

    (University of Bayreuth)

  • Renate Gelfert

    (University of Bayreuth)

  • Jennifer Kaiser

    (University of Bayreuth)

  • Veniamin Borin

    (The Hebrew University of Jerusalem)

  • Christian Renzl

    (University of Bonn)

  • Sebastian Pilsl

    (University of Bonn)

  • Américo Tavares Ranzani

    (University of Bayreuth)

  • Andrés García de Fuentes

    (University of Bayreuth)

  • Tobias Gleichmann

    (Humboldt-University Berlin)

  • Ralph P. Diensthuber

    (Humboldt-University Berlin)

  • Michael Weyand

    (University of Bayreuth)

  • Günter Mayer

    (University of Bonn
    University of Bonn)

  • Igor Schapiro

    (The Hebrew University of Jerusalem)

  • Andreas Möglich

    (University of Bayreuth
    Humboldt-University Berlin
    Universität Bayreuth
    Universität Bayreuth)

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.

Suggested Citation

  • Julia Dietler & Renate Gelfert & Jennifer Kaiser & Veniamin Borin & Christian Renzl & Sebastian Pilsl & Américo Tavares Ranzani & Andrés García de Fuentes & Tobias Gleichmann & Ralph P. Diensthuber & , 2022. "Signal transduction in light-oxygen-voltage receptors lacking the active-site glutamine," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30252-4
    DOI: 10.1038/s41467-022-30252-4
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    References listed on IDEAS

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    1. Oskar Berntsson & Ralph P. Diensthuber & Matthijs R. Panman & Alexander Björling & Emil Gustavsson & Maria Hoernke & Ashley J. Hughes & Léocadie Henry & Stephan Niebling & Heikki Takala & Janne A. Iha, 2017. "Sequential conformational transitions and α-helical supercoiling regulate a sensor histidine kinase," Nature Communications, Nature, vol. 8(1), pages 1-8, December.
    2. Mineo Iseki & Shigeru Matsunaga & Akio Murakami & Kaoru Ohno & Kiyoshi Shiga & Kazuichi Yoshida & Michizo Sugai & Tetsuo Takahashi & Terumitsu Hori & Masakatsu Watanabe, 2002. "A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis," Nature, Nature, vol. 415(6875), pages 1047-1051, February.
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    4. Estella F. Yee & Ralph P. Diensthuber & Anand T. Vaidya & Peter P. Borbat & Christopher Engelhard & Jack H. Freed & Robert Bittl & Andreas Möglich & Brian R. Crane, 2015. "Signal transduction in light–oxygen–voltage receptors lacking the adduct-forming cysteine residue," Nature Communications, Nature, vol. 6(1), pages 1-10, December.
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    Cited by:

    1. Stefanie S. M. Meier & Elina Multamäki & Américo T. Ranzani & Heikki Takala & Andreas Möglich, 2024. "Leveraging the histidine kinase-phosphatase duality to sculpt two-component signaling," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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