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

Author:

Turnšek Jernej12345ORCID,Brunson John K67,Viedma Maria del Pilar Martinez8ORCID,Deerinck Thomas J9,Horák Aleš1011,Oborník Miroslav1011,Bielinski Vincent A12,Allen Andrew Ellis46ORCID

Affiliation:

1. Biological and Biomedical Sciences, The Graduate School of Arts and Sciences, Harvard University, Cambridge, United States

2. Department of Systems Biology, Harvard Medical School, Boston, United States

3. Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, United States

4. Integrative Oceanography Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, United States

5. Center for Research in Biological Systems, University of California San Diego, La Jolla, United States

6. Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, United States

7. Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, United States

8. Informatics, J. Craig Venter Institute, La Jolla, United States

9. National Center for Microscopy and Imaging Research, University of California San Diego, La Jolla, United States

10. Biology Centre CAS, Institute of Parasitology, České Budějovice, Czech Republic

11. University of South Bohemia, Faculty of Science, České Budějovice, Czech Republic

12. Synthetic Biology and Bioenergy, J. Craig Venter Institute, La Jolla, 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.

Funder

Gordon and Betty Moore Foundation

National Science Foundation

Biological and Environmental Research

National Institutes of Health

Czech Science Foundation

European Regional Development Fund

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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