Light-dependent single-cell heterogeneity in the chloroplast redox state regulates cell fate in a marine diatom

  1. Avia Mizrachi
  2. Shiri Graff van Creveld
  3. Orr H Shapiro
  4. Shilo Rosenwasser
  5. Assaf Vardi  Is a corresponding author
  1. Weizmann Institute of Science, Israel
  2. Institute for Postharvest and Food Sciences, Agricultural Research Organization, The Volcani Center, Israel

Abstract

Diatoms are photosynthetic microorganisms of great ecological and biogeochemical importance, forming vast blooms in aquatic ecosystems. However, we are still lacking fundamental understanding of how individual cells sense and respond to diverse stress conditions, and what acclimation strategies are employed during bloom dynamics. We investigated cellular responses to environmental stress at the single-cell level using the roGFP sensor targeted to various organelles in the diatom Phaeodactylum tricornutum. We detected cell-to-cell variability using flow cytometry cell sorting and a microfluidics system for live imaging of roGFP oxidation dynamics. Chloroplast-targeted roGFP exhibited a light-dependent, bi-stable oxidation pattern in response to H2O2 and high light, revealing distinct subpopulations of sensitive oxidized cells and resilient reduced cells. Early oxidation in the chloroplast preceded commitment to cell death, and can be used for sensing stress cues and regulating cell fate. We propose that light-dependent metabolic heterogeneity regulates diatoms' sensitivity to environmental stressors in the ocean.

Data availability

MATLAB script used for image analysis is available at GitHub, as referenced in the methods section: https://github.com/aviamiz/ITRIA

Article and author information

Author details

  1. Avia Mizrachi

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7724-9275
  2. Shiri Graff van Creveld

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Orr H Shapiro

    Department of Food Quality and Safety, Institute for Postharvest and Food Sciences, Agricultural Research Organization, The Volcani Center, Rishon LeZion, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3222-9809
  4. Shilo Rosenwasser

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Assaf Vardi

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    For correspondence
    assaf.vardi@weizmann.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7079-0234

Funding

Israel Science Foundation (712233)

  • Assaf Vardi

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

Reviewing Editor

  1. Dianne K Newman, California Institute of Technology, United States

Version history

  1. Received: April 16, 2019
  2. Accepted: June 18, 2019
  3. Accepted Manuscript published: June 24, 2019 (version 1)
  4. Version of Record published: August 5, 2019 (version 2)

Copyright

© 2019, Mizrachi 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. Avia Mizrachi
  2. Shiri Graff van Creveld
  3. Orr H Shapiro
  4. Shilo Rosenwasser
  5. Assaf Vardi
(2019)
Light-dependent single-cell heterogeneity in the chloroplast redox state regulates cell fate in a marine diatom
eLife 8:e47732.
https://doi.org/10.7554/eLife.47732

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https://doi.org/10.7554/eLife.47732