Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation

Jorge Tovar, Gloria Leon-Avila, Lidya B. Sanchez, Robert Sutak, Jan Tachezy, Mark van der Giezen, Manuel Hernandez, Miklos Muller, John M. Lucocq

    Research output: Contribution to journalArticle

    360 Citations (Scopus)

    Abstract

    Giardia intestinalis (syn. lamblia) is one of the most widespread intestinal protozoan pathogens worldwide, causing hundreds of thousands of cases of diarrhoea each year1. Giardia is a member of the diplomonads, often described as an ancient protist group whose primitive nature is suggested by the lack of typical eukaryotic organelles (for example, mitochondria, peroxisomes), the presence of a poorly developed endomembrane system and by their early branching in a number of gene phylogenies1, 2. The discovery of nuclear genes of putative mitochondrial ancestry in Giardia3, 4, 5, 6, 7 and the recent identification of mitochondrial remnant organelles in amitochondrial protists such as Entamoeba histolytica8, 9 and Trachipleistophora hominis10 suggest that the eukaryotic amitochondrial state is not a primitive condition but is rather the result of reductive evolution. Using an in vitro protein reconstitution assay and specific antibodies against IscS and IscU—two mitochondrial marker proteins involved in iron–sulphur cluster biosynthesis—here we demonstrate that Giardia contains mitochondrial remnant organelles (mitosomes) bounded by double membranes that function in iron–sulphur protein maturation. Our results indicate that Giardia is not primitively amitochondrial and that it has retained a functional organelle derived from the original mitochondrial endosymbiont.
    Original languageEnglish
    Pages (from-to)172-176
    Number of pages5
    JournalNature
    Volume426
    Issue number6963
    DOIs
    Publication statusPublished - 2003

    Fingerprint

    Iron-Sulfur Proteins
    Giardia
    Organelles
    Diplomonadida
    Entamoeba
    Giardia lamblia
    Peroxisomes
    Mitochondrial Genes
    Mitochondrial Proteins
    Genetic Association Studies
    Diarrhea
    Mitochondria
    Proteins
    Membranes
    Antibodies
    Genes

    Cite this

    Tovar, J., Leon-Avila, G., Sanchez, L. B., Sutak, R., Tachezy, J., van der Giezen, M., ... Lucocq, J. M. (2003). Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature, 426(6963), 172-176. https://doi.org/10.1038/nature01945
    Tovar, Jorge ; Leon-Avila, Gloria ; Sanchez, Lidya B. ; Sutak, Robert ; Tachezy, Jan ; van der Giezen, Mark ; Hernandez, Manuel ; Muller, Miklos ; Lucocq, John M. / Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. In: Nature. 2003 ; Vol. 426, No. 6963. pp. 172-176.
    @article{801e4b899ad64744bf8ada93027284f1,
    title = "Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation",
    abstract = "Giardia intestinalis (syn. lamblia) is one of the most widespread intestinal protozoan pathogens worldwide, causing hundreds of thousands of cases of diarrhoea each year1. Giardia is a member of the diplomonads, often described as an ancient protist group whose primitive nature is suggested by the lack of typical eukaryotic organelles (for example, mitochondria, peroxisomes), the presence of a poorly developed endomembrane system and by their early branching in a number of gene phylogenies1, 2. The discovery of nuclear genes of putative mitochondrial ancestry in Giardia3, 4, 5, 6, 7 and the recent identification of mitochondrial remnant organelles in amitochondrial protists such as Entamoeba histolytica8, 9 and Trachipleistophora hominis10 suggest that the eukaryotic amitochondrial state is not a primitive condition but is rather the result of reductive evolution. Using an in vitro protein reconstitution assay and specific antibodies against IscS and IscU—two mitochondrial marker proteins involved in iron–sulphur cluster biosynthesis—here we demonstrate that Giardia contains mitochondrial remnant organelles (mitosomes) bounded by double membranes that function in iron–sulphur protein maturation. Our results indicate that Giardia is not primitively amitochondrial and that it has retained a functional organelle derived from the original mitochondrial endosymbiont.",
    author = "Jorge Tovar and Gloria Leon-Avila and Sanchez, {Lidya B.} and Robert Sutak and Jan Tachezy and {van der Giezen}, Mark and Manuel Hernandez and Miklos Muller and Lucocq, {John M.}",
    note = "dc.publisher: Nature Publishing Group dc.description.sponsorship: We thank G. Clark, J. Bowyer and S. Cutting for critically reading the manuscript. A recombinant plasmid containing the T. vaginalis ferredoxin gene was provided by J. P. Germanas and K. Krause. The use of partial genome sequence information from the Giardia Genome Project Database26 is acknowledged. The technical assistance of J. James and N. Sommerville is also acknowledged. M.H. is a sabbatical visitor supported by CINVESTAV, M{\'e}xico. Research at the Rockefeller University (gene cloning, antibody generation) was supported by a NIH grant to M.M. Research at Charles University (in vitro assembly of Fe–S clusters) was supported by a grant from FIRCA to J.Tachezy. J.M.L. (electron microscopy) was supported by a Research Leave Fellowship from the Wellcome Trust and by Tenovus Scotland. Research at Royal Holloway (bioinformatics, cell fractionation, fluorescence confocal microscopy, manuscript writing, project coordination) was supported by a Wellcome Trust grant to J.Tovar.",
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    Tovar, J, Leon-Avila, G, Sanchez, LB, Sutak, R, Tachezy, J, van der Giezen, M, Hernandez, M, Muller, M & Lucocq, JM 2003, 'Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation', Nature, vol. 426, no. 6963, pp. 172-176. https://doi.org/10.1038/nature01945

    Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. / Tovar, Jorge; Leon-Avila, Gloria; Sanchez, Lidya B.; Sutak, Robert; Tachezy, Jan; van der Giezen, Mark; Hernandez, Manuel; Muller, Miklos; Lucocq, John M.

    In: Nature, Vol. 426, No. 6963, 2003, p. 172-176.

    Research output: Contribution to journalArticle

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    T1 - Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation

    AU - Tovar, Jorge

    AU - Leon-Avila, Gloria

    AU - Sanchez, Lidya B.

    AU - Sutak, Robert

    AU - Tachezy, Jan

    AU - van der Giezen, Mark

    AU - Hernandez, Manuel

    AU - Muller, Miklos

    AU - Lucocq, John M.

    N1 - dc.publisher: Nature Publishing Group dc.description.sponsorship: We thank G. Clark, J. Bowyer and S. Cutting for critically reading the manuscript. A recombinant plasmid containing the T. vaginalis ferredoxin gene was provided by J. P. Germanas and K. Krause. The use of partial genome sequence information from the Giardia Genome Project Database26 is acknowledged. The technical assistance of J. James and N. Sommerville is also acknowledged. M.H. is a sabbatical visitor supported by CINVESTAV, México. Research at the Rockefeller University (gene cloning, antibody generation) was supported by a NIH grant to M.M. Research at Charles University (in vitro assembly of Fe–S clusters) was supported by a grant from FIRCA to J.Tachezy. J.M.L. (electron microscopy) was supported by a Research Leave Fellowship from the Wellcome Trust and by Tenovus Scotland. Research at Royal Holloway (bioinformatics, cell fractionation, fluorescence confocal microscopy, manuscript writing, project coordination) was supported by a Wellcome Trust grant to J.Tovar.

    PY - 2003

    Y1 - 2003

    N2 - Giardia intestinalis (syn. lamblia) is one of the most widespread intestinal protozoan pathogens worldwide, causing hundreds of thousands of cases of diarrhoea each year1. Giardia is a member of the diplomonads, often described as an ancient protist group whose primitive nature is suggested by the lack of typical eukaryotic organelles (for example, mitochondria, peroxisomes), the presence of a poorly developed endomembrane system and by their early branching in a number of gene phylogenies1, 2. The discovery of nuclear genes of putative mitochondrial ancestry in Giardia3, 4, 5, 6, 7 and the recent identification of mitochondrial remnant organelles in amitochondrial protists such as Entamoeba histolytica8, 9 and Trachipleistophora hominis10 suggest that the eukaryotic amitochondrial state is not a primitive condition but is rather the result of reductive evolution. Using an in vitro protein reconstitution assay and specific antibodies against IscS and IscU—two mitochondrial marker proteins involved in iron–sulphur cluster biosynthesis—here we demonstrate that Giardia contains mitochondrial remnant organelles (mitosomes) bounded by double membranes that function in iron–sulphur protein maturation. Our results indicate that Giardia is not primitively amitochondrial and that it has retained a functional organelle derived from the original mitochondrial endosymbiont.

    AB - Giardia intestinalis (syn. lamblia) is one of the most widespread intestinal protozoan pathogens worldwide, causing hundreds of thousands of cases of diarrhoea each year1. Giardia is a member of the diplomonads, often described as an ancient protist group whose primitive nature is suggested by the lack of typical eukaryotic organelles (for example, mitochondria, peroxisomes), the presence of a poorly developed endomembrane system and by their early branching in a number of gene phylogenies1, 2. The discovery of nuclear genes of putative mitochondrial ancestry in Giardia3, 4, 5, 6, 7 and the recent identification of mitochondrial remnant organelles in amitochondrial protists such as Entamoeba histolytica8, 9 and Trachipleistophora hominis10 suggest that the eukaryotic amitochondrial state is not a primitive condition but is rather the result of reductive evolution. Using an in vitro protein reconstitution assay and specific antibodies against IscS and IscU—two mitochondrial marker proteins involved in iron–sulphur cluster biosynthesis—here we demonstrate that Giardia contains mitochondrial remnant organelles (mitosomes) bounded by double membranes that function in iron–sulphur protein maturation. Our results indicate that Giardia is not primitively amitochondrial and that it has retained a functional organelle derived from the original mitochondrial endosymbiont.

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    Tovar J, Leon-Avila G, Sanchez LB, Sutak R, Tachezy J, van der Giezen M et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature. 2003;426(6963):172-176. https://doi.org/10.1038/nature01945