Flavodiiron proteins 1-to-4 function in versatile combinations in O2 photoreduction in cyanobacteria

  1. Anita Isabel Santana Sanchez
  2. Daniel Solymosi
  3. Henna Mustila
  4. Luca Bersanini
  5. Eva-Mari Aro  Is a corresponding author
  6. Yagut Allahverdiyeva-Rinne  Is a corresponding author
  1. University of Turku, Finland
  2. University of Uppsala, Sweden
  3. Vrije Universiteit Amsterdam, Netherlands

Abstract

Flavodiiron proteins (FDPs) constitute a group of modular enzymes widespread in all life Domains. Synechocystis sp. PCC 6803 has four FDPs (Flv1-4), which are essential for the photoprotection of photosynthesis. A direct comparison of light-induced O2 reduction (Mehler-like reaction) under high (3% CO2, HC) and low (air level CO2, LC) inorganic carbon conditions demonstrated that the Flv1/Flv3 heterodimer is solely responsible for an efficient steady-state O2 photoreduction under HC, with flv2 and flv4 expression strongly down-regulated. Conversely, under LC conditions, Flv1/Flv3 acts only as a transient electron sink, due to the competing withdrawal of electrons by the highly induced NDH-1 complex. Further, in vivo evidence is provided indicating that Flv2/Flv4 contributes to the Mehler-like reaction when naturally expressed under LC conditions, or, when artificially overexpressed under HC. The O2 photoreduction driven by Flv2/Flv4 occurs down-stream of PSI in a coordinated manner with Flv1/Flv3 and supports slow and steady-state O2 photoreduction.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Anita Isabel Santana Sanchez

    Department of Biochemistry, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  2. Daniel Solymosi

    Department of Biochemistry, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  3. Henna Mustila

    Microbial Chemistry, University of Uppsala, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  4. Luca Bersanini

    Department of Physics and Astronomy, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Eva-Mari Aro

    Department of Biochemistry, University of Turku, Turku, Finland
    For correspondence
    evaaro@utu.fi
    Competing interests
    The authors declare that no competing interests exist.
  6. Yagut Allahverdiyeva-Rinne

    Department of Biochemistry, University of Turku, Turku, Finland
    For correspondence
    allahve@utu.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9262-1757

Funding

Suomen Akatemia (315119)

  • Yagut Allahverdiyeva-Rinne

NordForsk (82845)

  • Eva-Mari Aro
  • Yagut Allahverdiyeva-Rinne

Koneen Säätiö (7fa491)

  • Yagut Allahverdiyeva-Rinne

Suomen Akatemia (307335)

  • Eva-Mari Aro

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Version history

  1. Received: February 4, 2019
  2. Accepted: July 10, 2019
  3. Accepted Manuscript published: July 11, 2019 (version 1)
  4. Version of Record published: July 25, 2019 (version 2)

Copyright

© 2019, Santana Sanchez et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Anita Isabel Santana Sanchez
  2. Daniel Solymosi
  3. Henna Mustila
  4. Luca Bersanini
  5. Eva-Mari Aro
  6. Yagut Allahverdiyeva-Rinne
(2019)
Flavodiiron proteins 1-to-4 function in versatile combinations in O2 photoreduction in cyanobacteria
eLife 8:e45766.
https://doi.org/10.7554/eLife.45766

Share this article

https://doi.org/10.7554/eLife.45766

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