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.

Metrics

  • 526
    views
  • 69
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.