Divergent functions of two clades of flavodoxin in diatoms mitigate oxidative stress and iron limitation

Abstract

Phytoplankton rely on diverse mechanisms to adapt to the decreased iron bioavailability and oxidative stress-inducing conditions of today's oxygenated oceans, including replacement of the iron-requiring ferredoxin electron shuttle protein with a less-efficient iron-free flavodoxin under iron limiting conditions. And yet, diatoms transcribe flavodoxins in high-iron regions in contrast to other phytoplankton. Here, we show that the two clades of flavodoxins present within diatoms exhibit a functional divergence, with only clade II flavodoxins displaying the canonical role in acclimation to iron limitation. We created CRISPR/Cas9 knock-outs of the clade I flavodoxin from the model diatom Thalassiosira pseudonana and found these cell lines are hypersensitive to oxidative stress, while maintaining a wild-type response to iron limitation. Within natural diatom communities, clade I flavodoxin transcript abundance is regulated over the diel cycle rather than in response to iron availability, whereas clade II transcript abundances increase either in iron‑limiting regions or under artificially induced iron-limitation. The observed functional specialization of two flavodoxin variants within diatoms reiterates two major stressors associated with contemporary oceans and illustrates diatom strategies to flourish in diverse aquatic ecosystems.

Data availability

Sequencing data from cultures have been deposited in GEO under accession code GSE217467. All other relevant data supporting the findings of the study are available in this article and its Supplementary files.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Shiri Graff van Creveld

    School of Oceanography, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3445-3046
  2. Sacha N Coesel

    School of Oceanography, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Stephen Blaskowski

    School of Oceanography, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ryan D Groussman

    School of Oceanography, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Megan J Schatz

    School of Oceanography, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. E Virginia Armbrust

    School of Oceanography, University of Washington, Seattle, United States
    For correspondence
    armbrust@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7865-5101

Funding

Simons Foundation (426570SP)

  • E Virginia Armbrust

Simons Foundation (721244)

  • E Virginia Armbrust

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

Reviewing Editor

  1. Andrew Ellis Allen, University of California San Diego, United States

Version history

  1. Preprint posted: October 21, 2022 (view preprint)
  2. Received: October 23, 2022
  3. Accepted: June 5, 2023
  4. Accepted Manuscript published: June 6, 2023 (version 1)
  5. Version of Record published: June 22, 2023 (version 2)

Copyright

© 2023, Graff van Creveld 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. Shiri Graff van Creveld
  2. Sacha N Coesel
  3. Stephen Blaskowski
  4. Ryan D Groussman
  5. Megan J Schatz
  6. E Virginia Armbrust
(2023)
Divergent functions of two clades of flavodoxin in diatoms mitigate oxidative stress and iron limitation
eLife 12:e84392.
https://doi.org/10.7554/eLife.84392

Share this article

https://doi.org/10.7554/eLife.84392

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