Impact of energy limitations on function and resilience in long-wavelength photosystem II

  1. Stefania Viola  Is a corresponding author
  2. William Roseby
  3. Stefano Santabarbara
  4. Dennis Nürnberg
  5. Ricardo Assunção
  6. Holger Dau
  7. Julien Sellés
  8. Alain Boussac
  9. Andrea Fantuzzi
  10. A William Rutherford  Is a corresponding author
  1. Imperial College London, United Kingdom
  2. Consiglio Nazionale delle Ricerche, Italy
  3. Freie Universität Berlin, Germany
  4. Institut de Biologie Physico-Chimique, France
  5. CEA Saclay, France

Abstract

Photosystem II (PSII) uses the energy from red light to split water and reduce quinone, an energy-demanding process based on chlorophyll a (Chl-a) photochemistry. Two types of cyanobacterial PSII can use chlorophyll d (Chl-d) and chlorophyll f (Chl-f) to perform the same reactions using lower energy, far-red light. PSII from Acaryochloris marina has Chl-d replacing all but one of its 35 Chl-a, while PSII from Chroococcidiopsis thermalis, a facultative far-red species, has just 4 Chl-f and 1 Chl-d and 30 Chl-a. From bioenergetic considerations, the far-red PSII were predicted to lose photochemical efficiency and/or resilience to photodamage. Here, we compare enzyme turnover efficiency, forward electron transfer, back-reactions and photodamage in Chl-f-PSII, Chl-d-PSII and Chl-a-PSII. We show that: i) all types of PSII have a comparable efficiency in enzyme turnover; ii) the modified energy gaps on the acceptor side of Chl-d-PSII favour recombination via PD1+Phe- repopulation, leading to increased singlet oxygen production and greater sensitivity to high-light damage compared to Chl-a-PSII and Chl-f-PSII; iii) the acceptor-side energy gaps in Chl-f-PSII are tuned to avoid harmful back reactions, favouring resilience to photodamage over efficiency of light usage. The results are explained by the differences in the redox tuning of the electron transfer cofactors Phe and QA and in the number and layout of the chlorophylls that share the excitation energy with the primary electron donor. PSII has adapted to lower energy in two distinct ways, each appropriate for its specific environment but with different functional penalties.

Data availability

Data and materials availability: All data generated and analysed during this study have been included in the manuscript and supporting file and provided as Source Data files.

Article and author information

Author details

  1. Stefania Viola

    Department of Life Sciences, Imperial College London, London, United Kingdom
    For correspondence
    s.viola@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  2. William Roseby

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Stefano Santabarbara

    Photosyntesis Research Unit, Consiglio Nazionale delle Ricerche, Milan, Italy
    Competing interests
    The authors declare that no competing interests exist.
  4. Dennis Nürnberg

    Physics Department, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Ricardo Assunção

    Physics Department, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Holger Dau

    Physics Department, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Julien Sellés

    Institut de Biologie Physico-Chimique, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Alain Boussac

    CEA Saclay, Gif-Sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Andrea Fantuzzi

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. A William Rutherford

    Department of Life Sciences, Imperial College London, London, United Kingdom
    For correspondence
    a.rutherford@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3124-154X

Funding

Biotechnology and Biological Sciences Research Council (BB/R001383/1)

  • Stefania Viola
  • William Roseby
  • Andrea Fantuzzi
  • A William Rutherford

Biotechnology and Biological Sciences Research Council (BB/V002015/1)

  • Stefania Viola
  • William Roseby
  • Andrea Fantuzzi
  • A William Rutherford

Biotechnology and Biological Sciences Research Council (BB/R00921X)

  • Stefania Viola
  • William Roseby
  • Andrea Fantuzzi
  • A William Rutherford

Labex (ANR-11-LABX-0011-01)

  • Julien Sellés

French Infrastructure for Integrated Structural Biology (ANR-10-INBS-05)

  • Alain Boussac

Fondazione Cariplo (2016-0667)

  • Stefano Santabarbara

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

Reviewing Editor

  1. David M Kramer, Michigan State University, United States

Publication history

  1. Received: April 30, 2022
  2. Accepted: July 18, 2022
  3. Accepted Manuscript published: July 19, 2022 (version 1)

Copyright

© 2022, Viola 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. Stefania Viola
  2. William Roseby
  3. Stefano Santabarbara
  4. Dennis Nürnberg
  5. Ricardo Assunção
  6. Holger Dau
  7. Julien Sellés
  8. Alain Boussac
  9. Andrea Fantuzzi
  10. A William Rutherford
(2022)
Impact of energy limitations on function and resilience in long-wavelength photosystem II
eLife 11:e79890.
https://doi.org/10.7554/eLife.79890

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