Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Ferritin is used for iron storage in bloom-forming marine pennate diatoms

Nature volume 457, pages 467–470 (2009)Cite this article

Abstract

Primary productivity in 30–40% of the world’s oceans is limited by availability of the micronutrient iron1,2. Regions with chronically low iron concentrations are sporadically pulsed with new iron inputs by way of dust3 or lateral advection from continental margins4. Addition of iron to surface waters in these areas induces massive phytoplankton blooms dominated primarily by pennate diatoms5,6. Here we provide evidence that the bloom-forming pennate diatoms Pseudo-nitzschia and Fragilariopsis use the iron-concentrating protein, ferritin, to safely store iron. Ferritin has not been reported previously in any member of the Stramenopiles, a diverse eukaryotic lineage that includes unicellular algae, macroalgae and plant parasites. Phylogenetic analyses suggest that ferritin may have arisen in this small subset of diatoms through a lateral gene transfer. The crystal structure and functional assays of recombinant ferritin derived from Pseudo-nitzschia multiseries reveal a maxi-ferritin that exhibits ferroxidase activity and binds iron. The protein is predicted to be targeted to the chloroplast to control the distribution and storage of iron for proper functioning of the photosynthetic machinery. Abundance of Pseudo-nitzschia ferritin transcripts is regulated by iron nutritional status, and is closely tied to the loss and recovery of photosynthetic competence. Enhanced iron storage with ferritin allows the oceanic diatom Pseudo-nitzschia granii to undergo several more cell divisions in the absence of iron than the comparably sized, oceanic centric diatom Thalassiosira oceanica. Ferritin in pennate diatoms probably contributes to their success in chronically low-iron regions that receive intermittent iron inputs, and provides an explanation for the importance of these organisms in regulating oceanic CO2 over geological timescales7,8.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Tertiary crystal structure and ferroxidase site of Pseudo-nitzschia multiseries ferritin.
Figure 2: Growth characteristics and ferritin transcript abundance in Pseudo-nitzschia.
Figure 3: Ferritin phylogenetic tree.
Figure 4: Growth characteristics and ferritin transcript abundance in the oceanic diatoms P. granii and T. oceanica grown in iron-free continuous cultures.

Similar content being viewed by others

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Protein Data Bank

Data deposits

All sequences have been deposited in GenBank under accession codes FJ004953–FJ004969 and are listed in Supplementary Table 2. The coordinates of the apo and iron-soaked ferritin structures have been deposited in the Protein Data Bank under respective accession numbers 3E6R and 3E6S.

References

  1. Martin, J. H. & Fitzwater, S. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331, 341–343 (1988)

    Article  ADS  CAS  Google Scholar 

  2. Moore, J. K., Doney, S. C., Glover, D. M. & Fung, I. Y. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep-Sea Res. II 49, 463–507 (2002)

    Article  ADS  CAS  Google Scholar 

  3. Jickells, T. D. et al. Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308, 67–71 (2005)

    Article  ADS  CAS  Google Scholar 

  4. Lam, P. J. & Bishop, J. K. B. The continental margin is a key source of iron to the HNLC North Pacific Ocean. Geophys. Res. Lett. 35 L07608 doi: 10.1029/2008GL033294 (2008)

    Article  ADS  CAS  Google Scholar 

  5. Marchetti, A., Sherry, N. D., Kiyosawa, H., Tsuda, A. & Harrison, P. J. Phytoplankton processes during a mesoscale iron enrichment in the NE subarctic Pacific: Part I – biomass and assemblage. Deep-Sea Res. II 53, 2095–2113 (2006)

    Article  ADS  Google Scholar 

  6. de Baar, H. J. W. et al. Synthesis of iron fertilization experiments: From the iron age in the age of enlightenment. J. Geophys. Res. 110 C09S16 doi: 10.1029/2004JC002601 (2005)

    Article  CAS  Google Scholar 

  7. Cortese, G. & Gersonde, R. Morphometric variability in the diatom Fragilariopsis kerguelensis: Implications for Southern Ocean paleoceanography. Earth Planet. Sci. Lett. 257, 526–544 (2007)

    Article  ADS  CAS  Google Scholar 

  8. Katsuki, K. & Takahashi, K. Diatoms as paleoenvironmental proxies for seasonal productivity, sea-ice and surface circulation in the Bering Sea during the late Quaternary. Deep-Sea Res. II 52, 2110–2130 (2005)

    Article  ADS  Google Scholar 

  9. Liu, X. & Theil, E. C. Ferritins: Dynamic management of biological iron and oxygen chemistry. Acc. Chem. Res. 38, 167–175 (2005)

    Article  CAS  Google Scholar 

  10. Gruber, A. et al. Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol. Biol. 64, 519–530 (2007)

    Article  CAS  Google Scholar 

  11. Jin, W., Takagi, H., Pancorbo, B. & Theil, E. C. “Opening” the ferritin pore for iron release by mutation of conserved amino acids at interhelix and loop sites. Biochemistry 40, 7525–7532 (2001)

    Article  CAS  Google Scholar 

  12. Yang, X. O., Chen-Barret, Y., Arosio, P. & Chasteen, N. D. Reaction paths of iron oxidation and hydrolysis in horse spleen and recombinant human ferritins. Biochemistry 37, 9743–9750 (1998)

    Article  CAS  Google Scholar 

  13. Xu, B. & Chasteen, N. D. Iron-oxidation chemistry in ferritin. J. Biol. Chem. 266, 19965–19970 (1991)

    CAS  PubMed  Google Scholar 

  14. Bou-Abdallah, F., Lewin, A. C., Le Brun, N. E., Moore, G. R. & Chasteen, N. D. Iron detoxification properties of Escherichia coli bacterioferritin — Attenuation of oxyradical chemistry. J. Biol. Chem. 277, 37064–37069 (2002)

    Article  CAS  Google Scholar 

  15. Yang, X., Chiacone, E., Stefanini, S., llari, A. & Chasteen, N. D. Iron oxidation and hydrolysis reactions of a novel ferritin from Listeria innocua . Biochem. J. 349, 783–786 (2000)

    Article  CAS  Google Scholar 

  16. Marchetti, A., Maldonado, M. T., Lane, E. S. & Harrison, P. J. Iron requirements of the pennate diatom Pseudo-nitzschia: Comparison of oceanic (HNLC) and coastal species. Limnol. Oceanogr. 51, 2092–2101 (2006)

    Article  ADS  CAS  Google Scholar 

  17. Sunda, W. G., Swift, D. G. & Huntsman, S. A. Low iron requirement for growth in oceanic phytoplankton. Nature 351, 55–57 (1991)

    Article  ADS  CAS  Google Scholar 

  18. Bowie, A. R. et al. The fate of added iron during a mesoscale fertilisation experiment in the Southern Ocean. Deep-Sea Res. II 48, 2703–2743 (2001)

    Article  ADS  CAS  Google Scholar 

  19. La Fontaine, S. et al. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii . Eukaryot. Cell 1, 736–757 (2002)

    Article  CAS  Google Scholar 

  20. Phaeodactylum. tricornutum v2.0. 〈http://genome.jgi-psf.org/Phatr2/Phatr2.home.html〉 (2006)

  21. Armbrust, E. V. et al. The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306, 79–86 (2004)

    Article  ADS  CAS  Google Scholar 

  22. Sims, P. A., Mann, D. G. & Medlin, L. K. Evolution of the diatoms: Insights from fossil, biological and molecular data. Phycologia 45, 361–402 (2006)

    Article  Google Scholar 

  23. Andersson, J. O. Lateral gene transfer in eukaryotes. Cell. Mol. Life Sci. 62, 1182–1197 (2005)

    Article  ADS  CAS  Google Scholar 

  24. Kustka, A. B., Allen, A. E. & Morel, F. M. M. Sequence analysis and transcriptional regulation of iron acquisition genes in two marine diatoms. J. Phycol. 43, 715–729 (2007)

    Article  CAS  Google Scholar 

  25. Maldonado, M. T. & Price, N. M. Influence of N substrate on Fe requirements of marine centric diatoms. Mar. Ecol. Prog. Ser. 141, 161–172 (1996)

    Article  ADS  CAS  Google Scholar 

  26. Sunda, W. & Huntsman, S. A. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem. 50, 189–206 (1995)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank S. S. Bates for providing P. multiseries CLN-47 and CLN-17 isolates used in this study, and T. Rynearson for sea water from OSP in which P. granii (UWOSP36) was isolated. We are grateful to K. R. Boissonneault for providing P. multiseries actin sequences, R. Marohl and I. Oleinkov for assistance with culture maintenance and sample analyses, and W. C. Lee for assistance with X-ray diffraction data collection. This study was supported by a Gordon and Betty Moore Foundation Marine Microbiology Investigator Award, National Science Foundation grants and a National Institute of Environmental Health Sciences grant to E.V.A.; a National Sciences and Engineering Research Council of Canada grant to M.T.M.; and a Canadian Institutes of Health Research grant to M.E.P.M. Portions of this research were carried out at the Canadian Light Source (CLS) and the Stanford Synchrotron Radiation Laboratory (SSRL). SSRL is a national user facility operated by Stanford University on behalf of the US Department of Energy, Office of Basic Energy Sciences. The SSRL Structural Molecular Biology Program is supported by the Department of Energy, Office of Biological and Environmental Research, and by the National Institutes of Health, National Center for Research Resources, Biomedical Technology Program, and the National Institute of General Medical Sciences.

Author Contributions A.M., M.S.P. and E.V.A. designed the study; A.M. and M.S.P. performed the FTN annotation, phylogeny analyses and conducted the FTN expression and continuous culture experiments; M.E.P.M. and M.T.M. guided—and L.P.M. and A.A. conducted—the ferritin protein crystallography and biochemical characterization experiments; E.O.L. assisted with sequencing and performed FTN surveys; F.R. performed flow cytometry analyses and assisted with culture experiments; A.M. wrote the paper with assistance from E.V.A., M.S.P., L.P.M., M.T.M., A.A. and M.E.P.M. All authors discussed the results and commented on the manuscript.

Author information

Author notes

  1. Adrian Marchetti and Micaela S. Parker: These authors contributed equally to this work.

Authors and Affiliations

  1. School of Oceanography, University of Washington, Box 357940, Seattle, Washington 98195, USA ,

    Adrian Marchetti, Micaela S. Parker, Ellen O. Lin, Francois Ribalet & E. Virginia Armbrust

  2. Department of Earth and Ocean Sciences, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada,

    Lauren P. Moccia & Maria T. Maldonado

  3. Department of Microbiology and Immunology, University of British Columbia, 2350 Health Sciences Mall, Vancouver, British Columbia V6T 1Z3, Canada,

    Angele L. Arrieta & Michael E. P. Murphy

Authors
  1. Adrian Marchetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Micaela S. Parker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lauren P. Moccia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ellen O. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Angele L. Arrieta
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Francois Ribalet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael E. P. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria T. Maldonado
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. E. Virginia Armbrust
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Virginia Armbrust.

Supplementary information

Supplementary Information

This file contains Supplementary Tables S1-S6, Supplementary Figures S1-S7 and Legends, Supplementary Notes S1-S4, Supplementary Methods and Supplementary References. (PDF 1296 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marchetti, A., Parker, M., Moccia, L. et al. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457, 467–470 (2009). https://doi.org/10.1038/nature07539

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature07539

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing