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The photochemical mechanism of a B12-dependent photoreceptor protein

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  • Roger J. Kutta

    (School of Chemistry, The University of Manchester, Oxford Road
    Photon Science Institute, The University of Manchester
    SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester)

  • Samantha J. O. Hardman

    (SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester
    Faculty of Life Sciences, The University of Manchester, Carys Bannister Building, Dover Street)

  • Linus O. Johannissen

    (SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester
    Faculty of Life Sciences, The University of Manchester, Carys Bannister Building, Dover Street)

  • Bruno Bellina

    (School of Chemistry, The University of Manchester, Oxford Road
    SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester)

  • Hanan L. Messiha

    (SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester
    Faculty of Life Sciences, The University of Manchester, Carys Bannister Building, Dover Street)

  • Juan Manuel Ortiz-Guerrero

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

  • Montserrat Elías-Arnanz

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

  • S. Padmanabhan

    (Instituto de Química Física ‘Rocasolano’, Consejo Superior de Investigaciones Científicas)

  • Perdita Barran

    (School of Chemistry, The University of Manchester, Oxford Road
    SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester)

  • Nigel S. Scrutton

    (SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester
    Faculty of Life Sciences, The University of Manchester, Carys Bannister Building, Dover Street)

  • Alex R. Jones

    (School of Chemistry, The University of Manchester, Oxford Road
    Photon Science Institute, The University of Manchester
    SYNBIOCHEM, Manchester Institute of Biotechnology, The University of Manchester)

Abstract

The coenzyme B12-dependent photoreceptor protein, CarH, is a bacterial transcriptional regulator that controls the biosynthesis of carotenoids in response to light. On binding of coenzyme B12 the monomeric apoprotein forms tetramers in the dark, which bind operator DNA thus blocking transcription. Under illumination the CarH tetramer dissociates, weakening its affinity for DNA and allowing transcription. The mechanism by which this occurs is unknown. Here we describe the photochemistry in CarH that ultimately triggers tetramer dissociation; it proceeds via a cob(III)alamin intermediate, which then forms a stable adduct with the protein. This pathway is without precedent and our data suggest it is independent of the radical chemistry common to both coenzyme B12 enzymology and its known photochemistry. It provides a mechanistic foundation for the emerging field of B12 photobiology and will serve to inform the development of a new class of optogenetic tool for the control of gene expression.

Suggested Citation

  • Roger J. Kutta & Samantha J. O. Hardman & Linus O. Johannissen & Bruno Bellina & Hanan L. Messiha & Juan Manuel Ortiz-Guerrero & Montserrat Elías-Arnanz & S. Padmanabhan & Perdita Barran & Nigel S. Sc, 2015. "The photochemical mechanism of a B12-dependent photoreceptor protein," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms8907
    DOI: 10.1038/ncomms8907
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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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