Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid<i>Neocallimastix</i>sp.

Voncken, Frank; Boxma, Brigitte; Tjaden, Joachim; Akhmanova, Anna; Huynen, Martijn A.; Verbeek, Fons J.; Tielens, Aloysius G.M.; Haferkamp, Ilka; Neuhaus, H. Ekkehard; Vogels, Godfried D.; Veenhuis, Marten; Hackstein, J.H.P.

doi:10.1046/j.1365-2958.2002.02959.x

Cited by 97 publications

(83 citation statements)

References 76 publications

(101 reference statements)

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“…Recombined homologs of PFO are present in the yeast genome (and many other fungal genomes) as sulfite reductase (200,419). ATP is exported from chytrid hydrogenosomes to the cytosol via an ATP-ADP translocase belonging to the mitochondrial carrier family (MCF) (523,545).…”

Section: Fungimentioning

confidence: 99%

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Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Müller

Mentel

Hellemond

et al. 2012

Microbiol Mol Biol Rev

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695

904

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SUMMARY Major insights into the phylogenetic distribution, biochemistry, and evolutionary significance of organelles involved in ATP synthesis (energy metabolism) in eukaryotes that thrive in anaerobic environments for all or part of their life cycles have accrued in recent years. All known eukaryotic groups possess an organelle of mitochondrial origin, mapping the origin of mitochondria to the eukaryotic common ancestor, and genome sequence data are rapidly accumulating for eukaryotes that possess anaerobic mitochondria, hydrogenosomes, or mitosomes. Here we review the available biochemical data on the enzymes and pathways that eukaryotes use in anaerobic energy metabolism and summarize the metabolic end products that they generate in their anaerobic habitats, focusing on the biochemical roles that their mitochondria play in anaerobic ATP synthesis. We present metabolic maps of compartmentalized energy metabolism for 16 well-studied species. There are currently no enzymes of core anaerobic energy metabolism that are specific to any of the six eukaryotic supergroup lineages; genes present in one supergroup are also found in at least one other supergroup. The gene distribution across lineages thus reflects the presence of anaerobic energy metabolism in the eukaryote common ancestor and differential loss during the specialization of some lineages to oxic niches, just as oxphos capabilities have been differentially lost in specialization to anoxic niches and the parasitic life-style. Some facultative anaerobes have retained both aerobic and anaerobic pathways. Diversified eukaryotic lineages have retained the same enzymes of anaerobic ATP synthesis, in line with geochemical data indicating low environmental oxygen levels while eukaryotes arose and diversified.

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Section: Fungimentioning

confidence: 99%

“…The ATP generated in trichomonad hydrogenosomes is thought to reach the cytosol via a mitochondrial-type ADP/ATP carrier homolog, Hmp31 (126,545). The spectrum of mitochondrial carrier family (MCF) proteins is remarkably small, in addition to the ATP/ADP carrier.…”

Section: Fig 11mentioning

confidence: 99%

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Müller

Mentel

Hellemond

et al. 2012

Microbiol Mol Biol Rev

Self Cite

695

904

View full text Add to dashboard Cite

show abstract

“…The evidence for common ancestry of chytrid and ciliate hydrogenosomes with mitochondria is now very strong (van der Voncken et al 2002a;Boxma et al 2005). Among ciliates, mitochondria-and hydrogenosome-containing groups freely intermingle; there are at least four and probably more ciliate lineages that possess hydrogenosomes within this predominantly aerobic group (Fenchel & Finlay 1995;Embley et al 1995).…”

Section: Hydrogenosomes: Mitochondria That Make Hydrogenmentioning

confidence: 99%

“…Neocallimastix also contains a member of the MCF on its genome (van der Voncken et al 2002a). This protein has been shown to import and export ADP and ATP in vitro and, crucially, it can restore the function of mutant yeast mitochondria that lack their own ADP/ ATP carrier (van der .…”

Section: Hydrogenosomes: Mitochondria That 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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“…Multiple granular organelles, the hydrogenosomes, are characteristic of T. vaginalis and are involved in the parasite's metabolic pathways. The origin of the hydrogenosome remains under debate and is believed to be either analogous with the mitochondria having shared a common ancestor, the a-Gram negative proteobacteria [9], or alternatively, a direct derivative of the mitochondrion itself [10]. T. vaginalis trophozoites divide via longitudinal binary fission.…”

Section: Introductionmentioning

confidence: 99%

Drug resistance in the sexually transmitted protozoan Trichomonas vaginalis

et al. 2003

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Trichomoniasis is the most common, sexually transmitted infection. It is caused by the flagellated protozoan parasite Trichomonas vaginalis. Symptoms include vaginitis and infections have been associated with preterm delivery, low birth weight and increased infant mortality, as well as predisposing to HIV/AIDS and cervical cancer. Trichomoniasis has the highest prevalence and incidence of any sexually transmitted infection. The 5-nitroimidazole drugs, of which metronidazole is the most prescribed, are the only approved, effective drugs to treat trichomoniasis. Resistance against metronidazole is frequently reported and cross-resistance among the family of 5-nitroimidazole drugs is common, leaving no alternative for treatment, with some cases remaining unresolved. The mechanism of metronidazole resistance in T. vaginalis from treatment failures is not well understood, unlike resistance which is developed in the laboratory under increasing metronidazole pressure. In the latter situation, hydrogenosomal function which is involved in activation of the prodrug, metronidazole, is down-regulated. Reversion to sensitivity is incomplete after removal of drug pressure in the highly resistant parasites while clinically resistant strains, so far analysed, maintain their resistance levels in the absence of drug pressure. Although anaerobic resistance has been regarded as a laboratory induced phenomenon, it clearly has been demonstrated in clinical isolates. Pursuit of both approaches will allow dissection of the underlying mechanisms. Many alternative drugs and treatments have been tested in vivo in cases of refractory trichomoniasis, as well as in vitro with some successes including the broad spectrum anti-parasitic drug nitazoxanide. Drug resistance incidence in T. vaginalis appears to be on the increase and improved surveillance of treatment failures is urged.

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Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytridNeocallimastixsp.

Cited by 97 publications

References 76 publications

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Drug resistance in the sexually transmitted protozoan Trichomonas vaginalis

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