Reductive Evolution of the Mitochondrial Processing Peptidases of the Unicellular Parasites Trichomonas vaginalis and Giardia intestinalis

Šmíd, Ondřej; Matušková, Anna; Harris, Simon R.; Kučera, Tomáš; Novotný, Marián; Horváthová, Lenka; Hrdý, Ivan; Kutějová, Eva; Hirt, Robert P.; Embley, T. Martin; Janata, Jiřı́; Tachezy, Jan

doi:10.1371/journal.ppat.1000243

Cited by 56 publications

(64 citation statements)

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“…In other anaerobic eukaryotes, protein import machinery to the mitochondrion-related organelles appears to be conserved (43,44), and the mitosomal targeting signal from G. lamblia and the hydrogenosome targeting signal from T. vaginalis were interchangeable (45). On the contrary, cryptic mitochondrial targeting signals have also been discovered in G. lamblia, T. vaginalis, and microsporidian species, and unique aspects of mitochondrial processing peptidases have been reported in G. lamblia (1,46). Together, the machinery and mechanisms of protein import into mitosomes require further investigation.…”

Section: Discussionmentioning

confidence: 99%

Mitosomes in Entamoeba histolytica contain a sulfate activation pathway

Mi-ichi

Yousuf

Nakada‐Tsukui

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

127

251

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Hydrogenosomes and mitosomes are mitochondrion-related organelles in anaerobic/microaerophilic eukaryotes with highly reduced and divergent functions. The full diversity of their content and function, however, has not been fully determined. To understand the central role of mitosomes in Entamoeba histolytica, a parasitic protozoon that causes amoebic dysentery and liver abscesses, we examined the proteomic profile of purified mitosomes. Using 2 discontinuous Percoll gradient centrifugation and MS analysis, we identified 95 putative mitosomal proteins. Immunofluorescence assay showed that 3 proteins involved in sulfate activation, ATP sulfurylase, APS kinase, and inorganic pyrophosphatase, as well as sodium/sulfate symporter, involved in sulfate uptake, were compartmentalized to mitosomes. We have also provided biochemical evidence that activated sulfate derivatives, adenosine-5-phosphosulfate and 3-phosphoadenosine-5-phosphosulfate, were produced in mitosomes. Phylogenetic analysis showed that the aforementioned proteins and chaperones have distinct origins, suggesting the mosaic character of mitosomes in E. histolytica consisting of proteins derived from ␣-proteobacterial, ␦-proteobacterial, and ancestral eukaryotic origins. These results suggest that sulfate activation is the major function of mitosomes in E. histolytica and that E. histolytica mitosomes represent a unique mitochondrion-related organelle with remarkable diversity.anaerobic protozoa ͉ evolution ͉ mitochondria ͉ organelle ͉ proteomics D iversification of mitochondrial structure and function has occurred during eukaryotic evolution, and was especially observed in anaerobic/microaerophilic environments. Most extant anaerobic eukaryotes, which were previously considered to lack mitochondria, are now regarded to possess reduced and highly divergent forms of mitochondrion-related organelles (1, 2). The hydrogenosome is an organelle in which hydrogen and ATP are produced, and is found in anaerobic protists and fungi such as Trichomonas vaginalis (3, 4), Neocallimastix patriciarum (5, 6), and Nyctotherus ovalis (7). The mitosome, typically demonstrated in parasitic and free-living protists such as E. histolytica (2,(8)(9)(10)(11)(12)(13)(14)(15), Giardia intestinalis (16, 17), diverse microsporidian species (18)(19)(20), and Cryptosporidium parvum (21), generally has reduced functions and does not produce hydrogen or ATP. In Mastigamoeba balamuthi, a mitochondrion-related organelle was discovered and presumed to possess a unique array of biochemical properties, although it remains unclear whether the organelle is more similar to either hydrogenosomes or mitosomes (22). In contrast, the mitochondrion-related organelle in Blastocystis contains DNA and shows characteristics for both hydrogenosomes and mitochondria of higher eukaryotes (23). Organisms that possess hydrogenosomes and mitosomes do not cluster together in eukaryote phylogenies, indicating that secondary losses and changes in mitochondrial functions have independently occurred multiple times i...

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Section: Discussionmentioning

confidence: 99%

Mitosomes in Entamoeba histolytica contain a sulfate activation pathway

Mi-ichi

Yousuf

Nakada‐Tsukui

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

127

251

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“…highly specific and ATP-dependent process, even though the protein is not predicted to possess a cleavable NTS, which is typical of hydrogenosomal matrix proteins (44,45).…”

Section: Figmentioning

confidence: 99%

N-Terminal Presequence-Independent Import of Phosphofructokinase into Hydrogenosomes of Trichomonas vaginalis

et al. 2015

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bMitochondrial evolution entailed the origin of protein import machinery that allows nuclear-encoded proteins to be targeted to the organelle, as well as the origin of cleavable N-terminal targeting sequences (NTS) that allow efficient sorting and import of matrix proteins. In hydrogenosomes and mitosomes, reduced forms of mitochondria with reduced proteomes, NTS-independent targeting of matrix proteins is known. Here, we studied the cellular localization of two glycolytic enzymes in the anaerobic pathogen Trichomonas vaginalis: PP i -dependent phosphofructokinase (TvPP i -PFK), which is the main glycolytic PFK activity of the protist, and ATP-dependent PFK (TvATP-PFK), the function of which is less clear. TvPP i -PFK was detected predominantly in the cytosol, as expected, while all four TvATP-PFK paralogues were imported into T. vaginalis hydrogenosomes, although none of them possesses an NTS. The heterologous expression of TvATP-PFK in Saccharomyces cerevisiae revealed an intrinsic capability of the protein to be recognized and imported into yeast mitochondria, whereas yeast ATP-PFK resides in the cytosol. TvATP-PFK consists of only a catalytic domain, similarly to "short" bacterial enzymes, while ScATP-PFK includes an N-terminal extension, a catalytic domain, and a C-terminal regulatory domain. Expression of the catalytic domain of ScATP-PFK and short Escherichia coli ATP-PFK in T. vaginalis resulted in their partial delivery to hydrogenosomes. These results indicate that TvATP-PFK and the homologous ATP-PFKs possess internal structural targeting information that is recognized by the hydrogenosomal import machinery. From an evolutionary perspective, the predisposition of ancient ATP-PFK to be recognized and imported into hydrogenosomes might be a relict from the early phases of organelle evolution.T he transition of the mitochondrion into an ATP-producing organelle was the crucial event at the eukaryote origin (1). ATP synthesis in eukaryotes is typically compartmentalized, with glycolysis in the cytosol and pyruvate oxidation in the mitochondria, which is linked to highly efficient oxidative phosphorylation (1, 2). In protists, however, there are notable exceptions to the usual scheme regarding both glycolysis and pyruvate oxidation. In Trichomonas vaginalis and other eukaryotes that possess an anaerobic form of mitochonria called hydrogenosomes, pyruvate is oxidized within the organelle via less efficient anaerobic fermentation (3). Giardia intestinalis, Entamoeba histolytica, and other eukaryotes possess a reduced form of mitochondria called mitosomes that do not produce ATP at all (4). In these organisms, pyruvate oxidation takes place exclusively in the cytosol (1). In kinetoplastids, glycolysis is compartmentalized in specialized microbodies called glycosomes (5). In some green algae, the first half of the glycolytic pathway is localized in the chloroplast (6, 7), while in the diatom Phaeodactylum tricornutum and other stramenopiles, several glycolytic enzymes are targeted to multiple compartments, such...

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“…Adapted from Tsaousis et al (2008). Copyright # Macmillan Publishers Ltd. (Tovar et al 2003) and protein import (Dolezal et al 2005;Regoes et al 2005;Š míd et al 2008) is unknown.…”

Section: All Mitochondrial Homologues Need To Make or Import Atpmentioning

confidence: 99%

“…The processing peptidases of Giardia and Trichomonas have recently been functionally characterized (Brown et al 2007;Š míd et al 2008). The Giardia MPP is so far unique in that it lacks the a-subunit and functions as a monomeric b-subunit (bGPP) (Š míd et al 2008).…”

Section: Protein Targetting and Protein Import (A) Presence Of Mitochmentioning

confidence: 99%

“…Chromalveolata, Stramenopiles mitochondria-like organelle DNA, [Fe]-hydrogenase , DNA, NAD7, b-SCS, PFOR (Wawrzyniak et al 2008), DNA N. ovalis Chromalveolata, Ciliophora hydrogenosome DNA and hydrogenase activity (Boxma et al 2005) T. vaginalis Excavata, Parabasalia hydrogenosome mtHsp70, mtHsp40, Cpn60, Cpn10, Pam18, Dyall et al 2003;Dolezal et al 2005), a and bMPP (Brown et al 2007;Š míd et al 2008), acetate:succinate CoA-transferases (van Grinsven et al 2008), succinyl CoA synthetase a-and b-subunits (Lahti et al 1994), adenylate kinase (Lange et al 1994), malic enzyme (Hrdy & Mü ller 1995b;Dyall et al 2004), ferredoxin, frataxin, Nfs, Isu (Sutak et al 2004;Dolezal et al 2005Dolezal et al , 2007 (Dyall et al 2000), Hmp35 (Dyall et al 2003), TrxR (Mentel et al 2008), flavodiiron protein (Smutna et al…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Diversity and reductive evolution of mitochondria among microbial eukaryotes

Hjort

Goldberg

Tsaousis

et al. 2010

Phil. Trans. R. Soc. B

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184

130

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All extant eukaryotes are now considered to possess mitochondria in one form or another. Many parasites or anaerobic protists have highly reduced versions of mitochondria, which have generally lost their genome and the capacity to generate ATP through oxidative phosphorylation. These organelles have been called hydrogenosomes, when they make hydrogen, or remnant mitochondria or mitosomes when their functions were cryptic. More recently, organelles with features blurring the distinction between mitochondria, hydrogenosomes and mitosomes have been identified. These organelles have retained a mitochondrial genome and include the mitochondrial-like organelle of Blastocystis and the hydrogenosome of the anaerobic ciliate Nyctotherus. Studying eukaryotic diversity from the perspective of their mitochondrial variants has yielded important insights into eukaryote molecular cell biology and evolution. These investigations are contributing to understanding the essential functions of mitochondria, defined in the broadest sense, and the limits to which reductive evolution can proceed while maintaining a viable organelle.

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Reductive Evolution of the Mitochondrial Processing Peptidases of the Unicellular Parasites Trichomonas vaginalis and Giardia intestinalis

Cited by 56 publications

References 35 publications

Mitosomes in Entamoeba histolytica contain a sulfate activation pathway

Mitosomes in Entamoeba histolytica contain a sulfate activation pathway

N-Terminal Presequence-Independent Import of Phosphofructokinase into Hydrogenosomes of Trichomonas vaginalis

Diversity and reductive evolution of mitochondria among microbial eukaryotes

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