A hydrogenosome with a genome

Akhmanova, Anna; Voncken, Frank; Alen, Theo van; Hoek, A. E. M. Van Den; Boxma, Brigitte; Vogels, Godfried D.; Veenhuis, Marten; Hackstein, J.H.P.

doi:10.1038/25023

Cited by 254 publications

(168 citation statements)

References 7 publications

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“…Hydrogenase genes have now been cloned from T. vaginalis Horner et al 2000), the ciliates N. ovalis (Akhmanova et al 1998) and Trimyema sp. (Embley et al 2003a), and the chytrid fungi Neocallimastix frontalis L2 and Piromyces sp.…”

Section: Evolutionary Origins Of the Enzymes Used To Make Hydrogenmentioning

confidence: 99%

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Embley

2006

Phil. Trans. R. Soc. B

111

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Classical ideas for early eukaryotic evolution often posited a period of anaerobic evolution producing a nucleated phagocytic cell to engulf the mitochondrial endosymbiont, whose presence allowed the host to colonize emerging aerobic environments. This idea was given credence by the existence of contemporary anaerobic eukaryotes that were thought to primitively lack mitochondria, thus providing examples of the type of host cell needed. However, the groups key to this hypothesis have now been shown to contain previously overlooked mitochondrial homologues called hydrogenosomes or mitosomes; organelles that share common ancestry with mitochondria but which do not carry out aerobic respiration. Mapping these data on the unfolding eukaryotic tree reveals that secondary adaptation to anaerobic habitats is a reoccurring theme among eukaryotes. The apparent ubiquity of mitochondrial homologues bears testament to the importance of the mitochondrial endosymbiosis, perhaps as a founding event, in eukaryotic evolution. Comparative study of different mitochondrial homologues is needed to determine their fundamental importance for contemporary eukaryotic cells.

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Section: Evolutionary Origins Of the Enzymes Used To Make Hydrogenmentioning

confidence: 99%

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Embley

2006

Phil. Trans. R. Soc. B

111

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“…Currently, several lines of evidence support a common endosymbiotic ancestry for hydrogenosomes and mitochondria, despite their distinct metabolic pathways (3,5,6). Although the origin of hydrogenosomes within ciliate and fungi lineages is debated, these lineages branch with mitochondria-containing groups and the hydrogenosomes confined therein exhibit strong similarity to ciliate and fungal mitochondria (7,8).…”

mentioning

confidence: 99%

Trichomonas vaginalis Hmp35, a Putative Pore-forming Hydrogenosomal Membrane Protein, Can Form a Complex in Yeast Mitochondria

Dyall¹,

Lester

Schneider

et al. 2003

Journal of Biological Chemistry

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An abundant integral membrane protein, Hmp35, has been isolated from hydrogenosomes of Trichomonas vaginalis. This protein has no known homologue and exists as a stable 300-kDa complex, termed HMP35, in membranes of the hydrogenosome. By using blue native gel electrophoresis, we found the HMP35 complex to be stable in 2 M NaCl and up to 5 M urea. The endogenous Hmp35 protein was largely protease-resistant. The protein has a predominantly ␤-sheet structure and predicted transmembrane domains that may form a pore. Interestingly, the protein has a high number of cysteine residues, some of which are arranged in motifs that resemble the RING finger, suggesting that they could be coordinating zinc or another divalent cation. Our data show that Hmp35 forms one intramolecular but no intermolecular disulfide bonds. We have isolated the HMP35 complex by expressing a His-tagged Hmp35 protein in vivo followed by purification with nickel-agarose beads. The purified 300-kDa complex consists of mostly Hmp35 with lesser amounts of 12-, 25-27-, and 32-kDa proteins. The stoichiometry of proteins in the complex indicates that Hmp35 exists as an oligomer. Hmp35 can be targeted heterologously into yeast mitochondria, despite the lack of homology with any yeast protein, demonstrating the compatibility of mitochondrial and hydrogenosomal protein translocation machineries.Trichomonas vaginalis is a deep-branching protist that lacks archetypal eukaryotic "aerobic" organelles, specifically mitochondria and peroxisomes. This microaerophilic human-infective parasite carries out fermentative carbohydrate metabolism within hydrogenosomes. Hydrogenosomes are bounded by double membranes and produce ATP by substrate level phosphorylation (1). Hydrogenosomes are also found in certain chytrids, ciliates, and fungi, in lineages that are phylogenetically distant to the Parabasalian lineage to which trichomonads belong (1-4). Currently, several lines of evidence support a common endosymbiotic ancestry for hydrogenosomes and mitochondria, despite their distinct metabolic pathways (3,5,6). Although the origin of hydrogenosomes within ciliate and fungi lineages is debated, these lineages branch with mitochondria-containing groups and the hydrogenosomes confined therein exhibit strong similarity to ciliate and fungal mitochondria (7,8).Trichomonad hydrogenosomes, on the other hand, are markedly less similar to mitochondria. These organelles lack a genome (9) which would have provided a means to investigate their endosymbiotic origin as has been elegantly and convincingly done for mitochondria (10). In lieu of this, we and others have attempted to define the relationship between trichomonad hydrogenosomes and mitochondria by examining the origin of their chaperonins, metabolic enzymes, and membrane proteins. Chaperonin genes, specifically heat shock protein (Hsp) 1 70, cpn60,, and the IscS enzyme, involved in FeS cluster formation (15) appear to have a mitochondrial origin. However, analyses of metabolic enzymes such as hydrogenase (16,17), which is typi...

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“…The discovery of a ciliate hydrogenosome with DNA that shows high sequence similarity with mitochondrial SSU rRNA genes from aerobic ciliates (Akhmanova et al, 1998) confirms the mitochondrial origin of hydrogenosomes.…”

Section: Discussionmentioning

confidence: 70%

The ‘primitive’ microaerophile Giardia intestinalis (syn. lamblia, duodenalis) has specialized membranes with electron transport and membrane-potential-generating functions

et al. 2002

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Here it is shown that the flagellated protozoon Giardia intestinalis, commonly regarded as an early branching eukaryote because of its lack of mitochondria, has membraneous structures that partition the cationic, membrane-potentialsensitive fluorophore rhodamine 123. This organism also reduces a tetrazolium fluorogen at discrete plasma-membrane-associated sites. That these functions occur in distinctive specialized membrane systems supports the growing evidence that G. intestinalis may not be primitive, but is derived from an aerobic, mitochondria-containing flagellate.Keywords : tetrazolium dye, lower eukaryotes, confocal laser scanning microscopy, rhodamine 123, mitochondria INTRODUCTIONSome amitochondriate microaerophilic (Paget et al., 1989 ;Paget & Lloyd, 1990 ;Biagini et al., 1997a) flagellated protozoa have, until recently, been considered to be ' ancient eukaryotes ' with ' primitive ' characteristics (i.e. they lack mitochondria, peroxisomes, nucleoli, have only rudimentary Golgi stacks and produce energy by characteristically anaerobic pathways ; Cavalier-Smith, 1987). Thus, the diplomonads, including Giardia intestinalis (syn. lamblia, duodenalis) and Hexamita inflata, and the parabasalia, e.g. Trichomonas vaginalis, are shown in textbook phylogenies (Madigan et al., 2000) as ' early branching ' eukaryotes. However, this view has been challenged (Embley & Hirt, 1998), as all three species (G. intestinalis, H. inflata and T. vaginalis) have been shown to have genes encoding mitochondrial proteins. Thus, it is suggested that their apparently deep-branching status is a consequence of more recent secondary evolutionary modifications of aerobic mitochondriate organisms. Hydrogenosomes, the redox-active organelles of the parabasalia (Mu$ ller, 1998 ;Humphreys et al., 1998), of anaerobic rumen ciliates (Embley et al., 1995) and chytrid fungi (Biagini et al., 1997d) living in anoxic sediments (Biagini et al., 1997b), are now also believed to have been derived from ancestral mitochondria (Biagini et al., 1997c ;Embley et al., 1997).Alternative scenarios for the possible interactions of archaeal and bacterial precursors giving syntrophic and then symbiotic associations have been proposed (Gupta & Golding, 1996 ;Martin & Mu$ ller, 1998 ; Lo! pezGarcia & Moreira, 1999). Here we show, for the first time, that G. intestinalis has a small number of specialized plasma-membrane-associated structures that selectively partition the cationic, membrane-potentialsensitive dye rhodamine 123. The same membrane is lined at its inner face by regions that have specialized areas which act as reducing sites for a tetrazolium fluorogen. METHODS Materials.Fetal calf serum was supplied by GibcoBRL, through Life Technologies. Tryptone was purchased from Becton-Dickinson and trypticase was purchased from BioMe! rieux. Rhodamine 123 and tetrabromorhodamine 123 were from Molecular Probes, through Cambridge Bioscience. 5-Cyano-2,3-ditolyl tetrazolium chloride (CTC) is a product of Polysciences, distributed through Park Scientific. Fixat...

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A hydrogenosome with a genome

Cited by 254 publications

References 7 publications

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Trichomonas vaginalis Hmp35, a Putative Pore-forming Hydrogenosomal Membrane Protein, Can Form a Complex in Yeast Mitochondria

The ‘primitive’ microaerophile Giardia intestinalis (syn. lamblia, duodenalis) has specialized membranes with electron transport and membrane-potential-generating functions

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