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

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.

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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.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Protein Data Bank

Data deposits

All sequences have been deposited in GenBank under accession codes FJ004953FJ004969 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.

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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.

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Correspondence to E. Virginia Armbrust.

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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)

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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

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