Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria

Authors

  • Barbora Maralikova,

    1. School of Biological Sciences, Royal Holloway University of London, Egham TW20 0EX, UK.
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  • Vahab Ali,

    1. Department of Parasitology, Gunma University Graduate School of Medicine, Maebashi, 371–8 511, Japan.
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    • Present addresses: Department of Biochemistry, Rajendra Memorial Research Institute of Medical Sciences, Agamkuan, Patna-800 007, India;

  • Kumiko Nakada-Tsukui,

    1. Department of Parasitology, Gunma University Graduate School of Medicine, Maebashi, 371–8 511, Japan.
    2. Department of Parasitology, National Institute of Infectious Diseases, Tokyo 162–8640, Japan.
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  • Tomoyoshi Nozaki,

    1. Department of Parasitology, Gunma University Graduate School of Medicine, Maebashi, 371–8 511, Japan.
    2. Department of Parasitology, National Institute of Infectious Diseases, Tokyo 162–8640, Japan.
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  • Mark Van Der Giezen,

    1. School of Biological Sciences, Royal Holloway University of London, Egham TW20 0EX, UK.
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    • Centre for Eukaryotic Evolutionary Microbiology, School of Biosciences, University of Exeter, Exeter, EX4 4QD, UK.

  • Katrin Henze,

    1. Institute of Botany III, Heinrich Heine University, 40225 Düsseldorf, Germany.
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  • Jorge Tovar

    1. School of Biological Sciences, Royal Holloway University of London, Egham TW20 0EX, UK.
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E-mail j.tovar@rhul.ac.uk; Tel. (+44) 1784 414159; Fax (+44) 1784 414224.

Summary

The assembly of vital reactive iron-sulfur (Fe-S) cofactors in eukaryotes is mediated by proteins inherited from the original mitochondrial endosymbiont. Uniquely among eukaryotes, however, Entamoeba and Mastigamoeba lack such mitochondrial-type Fe-S cluster assembly proteins and possess instead an analogous bacterial-type system acquired by lateral gene transfer. Here we demonstrate, using immunomicroscopy and biochemical methods, that beyond their predicted cytosolic distribution the bacterial-type Fe-S cluster assembly proteins NifS and NifU have been recruited to function within the relict mitochondrial organelles (mitosomes) of Entamoeba histolytica. Both Nif proteins are 10-fold more concentrated within mitosomes compared with their cytosolic distribution suggesting that active Fe-S protein maturation occurs in these organelles. Quantitative immunoelectron microscopy showed that amoebal mitosomes are minute but highly abundant cellular structures that occupy up to 2% of the total cell volume. In addition, protein colocalization studies allowed identification of the amoebal hydroperoxide detoxification enzyme rubrerythrin as a mitosomal protein. This protein contains functional Fe-S centres and exhibits peroxidase activity in vitro. Our findings demonstrate the role of analogous protein replacement in mitochondrial organelle evolution and suggest that the relict mitochondrial organelles of Entamoeba are important sites of metabolic activity that function in Fe-S protein-mediated oxygen detoxification.

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