Almost all organisms require iron as a co-factor in numerous metalloproteins
and enzymes. In particular, phytoplankton, which are aquatic, free-drifting,
single-celled organisms that can harvest energy from the sun, have an elevated
demand for iron due to the large role it plays in their photosynthetic
machinery. In 30-40% of the world's oceans iron concentrations are low enough
to limit the growth of phytoplankton (Martin and Fitzwater 1988; Moore et al.
2002). New sources of iron to these regions are sporadic and typically
include atmospheric dust deposition or weak upwelling of deep waters.
Data collected at SSRL Beam Lines 9.2, 7.1 and at the Canadian Light Source
allowed the determination of crystal structures of recombinant ferritin from
the marine pennate diatom, Pseudo-nitzschia multiseries (Figure 1). This
pennate diatom ferritin forms an assembly of 24 monomers forming a hollow
sphere with a diameter of approximately 120 Å, typical of the ferritin
family (Figure 2A). In plants and animals, ferritin stores up to 4500 iron
atoms as an iron oxide mineral and can release it on cellular demand (Liu and
Theil 2005). Cells thereby are protected from potential oxidative damage
resulting from the interaction of iron with reactive oxygen. Iron atoms are
bound at the ferroxidase centers where ferrous iron is oxidized by oxygen
(Figure 2B). The ferroxidase site has unique features suggesting that catalytic
activity is tuned for the specific needs of the diatom. Additional iron atoms
were found to trail from the ferroxidase center towards the hollow center of
the ferritin sphere where mineralization and storage of iron occurs.
This research was supported by a Gordon and Betty Moore Foundation Marine
Microbiology Investigator Award, a National Science Foundation grant, a
National Institute of Environmental Health Sciences grant, a National Sciences
and Engineering Research Council of Canada grant and a Canadian Institutes of
Health Research grant. Portions of this research were carried out at the
Canadian Light Source and the SSRL. 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.
Primary Citation
Marchetti A., Parker M.S., Moccia L.P., Lin E.O., Arrieta A.L., Ribalet F.,
Murphy M.E.P., Maldonado M.T., Armbrust E.V. (2009) Ferritin is used for iron
storage in bloom-forming marine pennate diatoms. Nature, 457, 467-470.
References
Boyd, P. W., T. Jickells, C. S. Law, S. Blain, E. A. Boyle, K. O. Buesseler, K.
H. Coale, J. J. Cullen, H. J. W. De Baar, M. Follows, M. Harvey, C. Lancelot,
M. Levasseur, N. P. J. Owens, R. Pollard, R. B. Rivkin, J. Sarmiento, V.
Schoemann, V. Smetacek, S. Takeda, A. Tsuda, S. Turner, and A. J. Watson. 2007.
Mesoscale iron enrichment experiments 1993-2005: Synthesis and future
directions. Science 315: 612-617.
Martin, J. H., and S. Fitzwater. 1988. Iron deficiency limits phytoplankton
growth in the north-east Pacific subarctic. Nature 331: 341-343.
Moore, J. K., S. C. Doney, D. M. Glover, and I. Y. Fung. 2002. Iron cycling and
nutrient-limitation patterns in surface waters of the World Ocean. Deep-Sea
Research II 49: 463-507.
Nelson, D. M., P. Treguer, M. A. Brzezinski, A. Leynaert, and B. Queguiner.
1995. Production and dissolution of biogenic silica in the ocean: Revised
global estimates, comparison with regional data and relationships to biogenic
sedimentation. Global Biogeochemical Cycles 9: 359-372.
Sims, P. A., D. G. Mann, and L. K. Medlin. 2006. Evolution of the diatoms:
insights from fossil, biological and molecular data. Phycologia 45:
361-402.
Phytoplankton that persist in these regions must be able to rapidly take up and
store iron when it is available and withstand long intervals of limited iron
supply. Storing iron in ferritin is one mechanism that enables these organisms
to persist through iron droughts. Ferritins are highly specialized iron
storage proteins present in many animals, plants and microorganisms. We
recently discovered ferritin in a subset of marine diatoms, a highly diverse
group of phytoplankton that account for approximately 20% of the total
biological uptake of carbon dioxide on the planet (Nelson et al. 1995). The
presence of ferritin had not previously been identified within any member of
the Stramenopiles, a diverse eukaryotic lineage which includes diatoms and
other unicellular algae, macroalgae and plant parasites. Thus far, genes
encoding ferritins have only been found in pennate diatoms, a more recent
lineage of diatoms that diverged from their centric diatom counterparts about
75 million years ago (Sims et al. 2006).
Figure 1:
A light micrograph of the marine pennate diatom Pseudo-nitzschia
multiseries. Shown are one whole cell and two partial cells connected at
the cell tips in a chain. The brown components of the cells are the
chloroplasts. Scale bar = 5
mm. (Image courtesy of K. Holtermann)
The identification of iron as a limiting nutrient to phytoplankton growth has
lead to a wave of large-scale iron-enrichment experiments performed in
iron-limited regions around the globe. A primary objective of these
experiments was to investigate whether more carbon dioxide is removed from the
atmosphere when the iron-induced phytoplankton blooms sink to the ocean floor
(Boyd et al. 2007). The dominance of ferritin-containing pennate diatoms during
most of these experiments is probably not coincidental but rather due in part
to high iron storage mediated through ferritin. We found that when placed in an
iron-free environment, an oceanic pennate diatom that contains ferritin
underwent more cell divisions based on stored iron than an oceanic centric
diatom species that putatively does not contain ferritin. The discovery of
ferritin in a subset of diatoms helps elucidate how some phytoplankton take
advantage of pulsed iron supplies by safely sequestering large amounts of iron
that support subsequent growth and divisions well after iron levels return to
low, ambient concentrations. This study provides an example of how a single
molecule such as ferritin may be influential in defining the success and
distributions of ecologically important groups of marine primary producers.
Figure 2:
Crystal structure and ferroxidase site of recombinant Pseudo-nizschia
multiseries ferritin. A, Crystal structure of P. multiseries
ferritin multimer (24mer). B, Crystal structure of P. multiseries
ferritin monomer. The ferritin core is representative of the right side of the
figure. Iron atoms are depicted as brown spheres and co-ordinating residues in
the ferroxidase center are highlighted as stick models.
SSRL is supported by the 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.