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Structural basis for gene regulation by a B12-dependent photoreceptor

Author

Listed:
  • Marco Jost

    (Massachusetts Institute of Technology)

  • Jésus Fernández-Zapata

    (Instituto de Química Física “Rocasolano”, Consejo Superior de Investigaciones Científicas)

  • María Carmen Polanco

    (Area of Genetics (Unidad Asociada al Instituto de Química Física “Rocasolano”, Consejo Superior de Investigaciones Científicas), Faculty of Biology, Universidad de Murcia)

  • Juan Manuel Ortiz-Guerrero

    (Area of Genetics (Unidad Asociada al Instituto de Química Física “Rocasolano”, Consejo Superior de Investigaciones Científicas), Faculty of Biology, Universidad de Murcia
    †Present address: MRC Protein Phosphorylation and Ubiquitylation Unit, University of Dundee, Dundee DD1 5EH, UK.)

  • Percival Yang-Ting Chen

    (Massachusetts Institute of Technology)

  • Gyunghoon Kang

    (Massachusetts Institute of Technology)

  • S. Padmanabhan

    (Instituto de Química Física “Rocasolano”, Consejo Superior de Investigaciones Científicas)

  • Montserrat Elías-Arnanz

    (Area of Genetics (Unidad Asociada al Instituto de Química Física “Rocasolano”, Consejo Superior de Investigaciones Científicas), Faculty of Biology, Universidad de Murcia)

  • Catherine L. Drennan

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Howard Hughes Medical Institute, Massachusetts Institute of Technology)

Abstract

Photoreceptor proteins enable organisms to sense and respond to light. The newly discovered CarH-type photoreceptors use a vitamin B12 derivative, adenosylcobalamin, as the light-sensing chromophore to mediate light-dependent gene regulation. Here we present crystal structures of Thermus thermophilus CarH in all three relevant states: in the dark, both free and bound to operator DNA, and after light exposure. These structures provide visualizations of how adenosylcobalamin mediates CarH tetramer formation in the dark, how this tetramer binds to the promoter −35 element to repress transcription, and how light exposure leads to a large-scale conformational change that activates transcription. In addition to the remarkable functional repurposing of adenosylcobalamin from an enzyme cofactor to a light sensor, we find that nature also repurposed two independent protein modules in assembling CarH. These results expand the biological role of vitamin B12 and provide fundamental insight into a new mode of light-dependent gene regulation.

Suggested Citation

  • Marco Jost & Jésus Fernández-Zapata & María Carmen Polanco & Juan Manuel Ortiz-Guerrero & Percival Yang-Ting Chen & Gyunghoon Kang & S. Padmanabhan & Montserrat Elías-Arnanz & Catherine L. Drennan, 2015. "Structural basis for gene regulation by a B12-dependent photoreceptor," Nature, Nature, vol. 526(7574), pages 536-541, October.
    • Handle: RePEc:nat:nature:v:526:y:2015:i:7574:d:10.1038_nature14950
    DOI: 10.1038/nature14950
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    Cited by:

    1. Shaowei Zhang & Laura N. Jeffreys & Harshwardhan Poddar & Yuqi Yu & Chuanyang Liu & Kaylee Patel & Linus O. Johannissen & Lingyun Zhu & Matthew J. Cliff & Cunyu Yan & Giorgio Schirò & Martin Weik & Mi, 2024. "Photocobilins integrate B12 and bilin photochemistry for enzyme control," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Harshwardhan Poddar & Ronald Rios-Santacruz & Derren J. Heyes & Muralidharan Shanmugam & Adam Brookfield & Linus O. Johannissen & Colin W. Levy & Laura N. Jeffreys & Shaowei Zhang & Michiyo Sakuma & J, 2023. "Redox driven B12-ligand switch drives CarH photoresponse," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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