Proximity proteomics in a marine diatom reveals a putative cell surface-to-chloroplast iron trafficking pathway

  1. Jernej Turnšek
  2. John K Brunson
  3. Maria del Pilar Martinez Viedma
  4. Thomas J Deerinck
  5. Aleš Horák
  6. Miroslav Oborník
  7. Vincent A Bielinski
  8. Andrew Ellis Allen  Is a corresponding author
  1. Harvard University, United States
  2. University of California San Diego, United States
  3. J. Craig Venter Institute, United States
  4. National Center for Microscopy and Imaging Research, University of California San Diego, United States
  5. Czech Academy of Sciences, Czech Republic
  6. J Craig Venter Institute, United States

Abstract

Iron is a biochemically critical metal cofactor in enzymes involved in photosynthesis, cellular respiration, nitrate assimilation, nitrogen fixation, and reactive oxygen species defense. Marine microeukaryotes have evolved a phytotransferrin-based iron uptake system to cope with iron scarcity, a major factor limiting primary productivity in the global ocean. Diatom phytotransferrin is endocytosed, however proteins downstream of this environmentally ubiquitous iron receptor are unknown. We applied engineered ascorbate peroxidase APEX2-based subcellular proteomics to catalog proximal proteins of phytotransferrin in the model marine diatom Phaeodactylum tricornutum. Proteins encoded by poorly characterized iron-sensitive genes were identified including three that are expressed from a chromosomal gene cluster. Two of them showed unambiguous colocalization with phytotransferrin adjacent to the chloroplast. Further phylogenetic, domain, and biochemical analyses suggest their involvement in intracellular iron processing. Proximity proteomics holds enormous potential to glean new insights into iron acquisition pathways and beyond in these evolutionarily, ecologically, and biotechnologically important microalgae.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files

The following previously published data sets were used

Article and author information

Author details

  1. Jernej Turnšek

    Biological and Biomedical Sciences, The Graduate School of Arts and Sciences, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. John K Brunson

    Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Maria del Pilar Martinez Viedma

    Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Thomas J Deerinck

    National Center for Microscopy and Imaging Research, University of California San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Aleš Horák

    Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. Miroslav Oborník

    Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  7. Vincent A Bielinski

    Synthetic Biology and Bioenergy, J Craig Venter Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Andrew Ellis Allen

    Integrative Oceanography Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, United States
    For correspondence
    aallen@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5911-6081

Funding

Gordon and Betty Moore Foundation (GBMF3828)

  • Andrew Ellis Allen

Gordon and Betty Moore Foundation (GBMF5006)

  • Andrew Ellis Allen

National Science Foundation (NSF-OCE-1756884)

  • Andrew Ellis Allen

National Science Foundation (NSF-MCB-1818390)

  • Andrew Ellis Allen

Biological and Environmental Research (DE-SC0018344)

  • Andrew Ellis Allen

Gordon and Betty Moore Foundation (GBMF4958)

  • Jernej Turnšek

National Institutes of Health (1F31ES030613-01)

  • John K Brunson

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

Reviewing Editor

  1. Christian S Hardtke, University of Lausanne, Switzerland

Publication history

  1. Received: October 16, 2019
  2. Accepted: February 15, 2021
  3. Accepted Manuscript published: February 16, 2021 (version 1)
  4. Accepted Manuscript updated: February 19, 2021 (version 2)
  5. Version of Record published: March 18, 2021 (version 3)

Copyright

© 2021, Turnšek 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. Jernej Turnšek
  2. John K Brunson
  3. Maria del Pilar Martinez Viedma
  4. Thomas J Deerinck
  5. Aleš Horák
  6. Miroslav Oborník
  7. Vincent A Bielinski
  8. Andrew Ellis Allen
(2021)
Proximity proteomics in a marine diatom reveals a putative cell surface-to-chloroplast iron trafficking pathway
eLife 10:e52770.
https://doi.org/10.7554/eLife.52770

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