Identification of distinct pH-and zeaxanthin-dependent quenching in LHCSR3 from Chlamydomonas reinhardtii

  1. Julianne M Troiano
  2. Federico Perozeni
  3. Raymundo Moya
  4. Luca Zuliani
  5. Kwangyrul Baek
  6. EonSeon Jin
  7. Stefano Cazzaniga
  8. Matteo Ballottari  Is a corresponding author
  9. Gabriela S Schlau-Cohen  Is a corresponding author
  1. Massachusetts Institute of Technology, United States
  2. University of Verona, Italy
  3. Hanyang University, Republic of Korea

Abstract

Under high light, oxygenic photosynthetic organisms avoid photodamage by thermally dissipating absorbed energy, which is called non-photochemical quenching. In green algae, a chlorophyll and carotenoid-binding protein, light-harvesting complex stress-related (LHCSR3), detects excess energy via a pH drop and serves as a quenching site. Using a combined in vivo and in vitro approach, we investigated quenching within LHCSR3 from Chlamydomonas reinhardtii. In vitro two distinct quenching processes, individually controlled by pH and zeaxanthin, were identified within LHCSR3. The pH-dependent quenching was removed within a mutant LHCSR3 that lacks the residues that are protonated to sense the pH drop. Observation of quenching in zeaxanthin-enriched LHCSR3 even at neutral pH demonstrated zeaxanthin-dependent quenching, which also occurs in other light-harvesting complexes. Either pH- or zeaxanthin-dependent quenching prevented the formation of damaging reactive oxygen species, and thus the two quenching processes may together provide different induction and recovery kinetics for photoprotection in a changing environment.

Data availability

Source data files have been provided for Figures 1A and 3.Single-molecule photon emission data for Figures 1B-D and 2 has been deposited on Zenodo.org and is available at 10.5281/zenodo.4306869

The following data sets were generated

Article and author information

Author details

  1. Julianne M Troiano

    Department of Chemistry, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Federico Perozeni

    Department of Biotechnology, University of Verona, Verona, Italy
    Competing interests
    The authors declare that no competing interests exist.
  3. Raymundo Moya

    Department of Chemistry, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Luca Zuliani

    Department of Biotechnology, University of Verona, Verona, Italy
    Competing interests
    The authors declare that no competing interests exist.
  5. Kwangyrul Baek

    Department of Life Science, Hanyang University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  6. EonSeon Jin

    Department of Life Science, Hanyang University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  7. Stefano Cazzaniga

    Department of Biotechnology, University of Verona, Verona, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2824-7916
  8. Matteo Ballottari

    Department of Biotechnology, University of Verona, Verona, Italy
    For correspondence
    matteo.ballottari@univr.it
    Competing interests
    The authors declare that no competing interests exist.
  9. Gabriela S Schlau-Cohen

    Department of Chemistry, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    gssc@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7746-2981

Funding

Human Frontiers Science Program (RGY0076)

  • Gabriela S Schlau-Cohen

National Science Foundation (CHE-1740645)

  • Gabriela S Schlau-Cohen

H2020 European Research Council (679814)

  • Matteo Ballottari

Korea Ministry of Science and ICT (NRF-2014M1A8A1049273)

  • EonSeon Jin

Arnold and Mabel Beckman Foundation (Postdoctoral Fellowship)

  • Julianne M Troiano

National Science Foundation (Graduate Research Fellowship)

  • Raymundo Moya

Arnold and Mabel Beckman Foundation (Beckman Young Investigator)

  • Gabriela S Schlau-Cohen

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

Version history

  1. Received: June 24, 2020
  2. Accepted: January 14, 2021
  3. Accepted Manuscript published: January 15, 2021 (version 1)
  4. Version of Record published: February 5, 2021 (version 2)

Copyright

© 2021, Troiano 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. Julianne M Troiano
  2. Federico Perozeni
  3. Raymundo Moya
  4. Luca Zuliani
  5. Kwangyrul Baek
  6. EonSeon Jin
  7. Stefano Cazzaniga
  8. Matteo Ballottari
  9. Gabriela S Schlau-Cohen
(2021)
Identification of distinct pH-and zeaxanthin-dependent quenching in LHCSR3 from Chlamydomonas reinhardtii
eLife 10:e60383.
https://doi.org/10.7554/eLife.60383

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