First published online July 9, 2004; 10.1104/pp.104.042770
Plant Physiology 135:1666-1673 (2004)
© 2004 American Society of Plant Biologists
ENVIRONMENTAL STRESS AND ADAPTATION
Critical Roles of Bacterioferritins in Iron Storage and Proliferation of Cyanobacteria1,[w]
Nir Keren*,
Rajeev Aurora and
Himadri B. Pakrasi
Department of Biology, Washington University, St. Louis, Missouri 63130
Cyanobacteria are key contributors to global photosynthetic productivity, and iron availability is essential for cyanobacterial proliferation. While iron is abundant in the earth's crust, its unique chemical properties render it a limiting factor for photoautotrophic growth. As compared to other nonphotosynthetic organisms, oxygenic photosynthetic organisms such as cyanobacteria, algae, and green plants need large amounts of iron to maintain functional PSI complexes in their photosynthetic apparatus. Ferritins and bacterioferritins are ubiquitously present iron-storage proteins. We have found that in the cyanobacterium Synechocystis sp. PCC 6803 (Synechocystis 6803), bacterioferritins are responsible for the storage of as much as 50% of cellular iron. Synechocystis 6803, as well as many other cyanobacterial species, have two bacterioferritins, BfrA and BfrB, in which either the heme binding or di-iron center ligating residues are absent. Purified bacterioferritin complex from Synechocystis 6803 has both BfrA and BfrB proteins. Targeted mutagenesis of each of the two bacterioferritin genes resulted in poor growth under iron-deprived conditions. Inactivation of both genes did not result in a more severe phenotype. These results support the presence of a heteromultimeric structure of Synechocystis bacterioferritin, in which one subunit ligates a di-iron center while the other accommodates heme binding. Notably, the reduced internal iron concentrations in the mutant cells resulted in a lower content of PSI. In addition, they triggered iron starvation responses even in the presence of normal levels of external iron, thus demonstrating a central role of bacterioferritins in iron homeostasis in these photosynthetic organisms.
1 This work was supported by grants from the U.S. Department of Energy, (USDA-NRI grant no. 00003348) and by the Department of Biology, Washington University, from funds provided by the Danforth Foundation. N.K. was partially supported by the International Human Frontier Science Program and The European Molecular Biology Organization.
[w] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.042770.
* Corresponding author; e-mail nir{at}biology2.wustl.edu; fax 314–935–6803.
Received March 15, 2004;
returned for revision May 4, 2004;
accepted May 5, 2004.
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