Deep Origin of Plastid/Parasite ATP/ADP Translocases

Amiri, Haleh; Karlberg, Olof; Andersson, Siv G. E.

doi:10.1007/s00239-002-2387-0

Cited by 55 publications

(46 citation statements)

References 59 publications

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“…For example, the mitochondrial ATP/ADP translocase that exports the ATP produced in the mitochondrion to the cytoplasm shows no sequence similarity to the bacterial type of ATP/ADP translocase. Rather, the mitochondrial ATP/ADP translocase has evolved from a family of eukaryotic phosphate transporters (19). Studies of the yeast mitochondrial proteome have indicated that about 40% of all mitochondrial proteins have no homologos in bacteria, and might thus have originated within the eukaryotic genome (20,21).…”

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confidence: 99%

Mitochondrial genomes are retained by selective constraints on protein targeting

Björkholm

Harish

Hagström

et al. 2015

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

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Mitochondria are energy-producing organelles in eukaryotic cells considered to be of bacterial origin. The mitochondrial genome has evolved under selection for minimization of gene content, yet it is not known why not all mitochondrial genes have been transferred to the nuclear genome. Here, we predict that hydrophobic membrane proteins encoded by the mitochondrial genomes would be recognized by the signal recognition particle and targeted to the endoplasmic reticulum if they were nuclear-encoded and translated in the cytoplasm. Expression of the mitochondrially encoded proteins Cytochrome oxidase subunit 1, Apocytochrome b, and ATP synthase subunit 6 in the cytoplasm of HeLa cells confirms export to the endoplasmic reticulum. To examine the extent to which the mitochondrial proteome is driven by selective constraints within the eukaryotic cell, we investigated the occurrence of mitochondrial protein domains in bacteria and eukaryotes. The accessory protein domains of the oxidative phosphorylation system are unique to mitochondria, indicating the evolution of new protein folds. Most of the identified domains in the accessory proteins of the ribosome are also found in eukaryotic proteins of other functions and locations. Overall, one-third of the protein domains identified in mitochondrial proteins are only rarely found in bacteria. We conclude that the mitochondrial genome has been maintained to ensure the correct localization of highly hydrophobic membrane proteins. Taken together, the results suggest that selective constraints on the eukaryotic cell have played a major role in modulating the evolution of the mitochondrial genome and proteome. mitochondria | protein domain | evolution | endoplasmatic reticulum | signal recognition particle

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confidence: 99%

Mitochondrial genomes are retained by selective constraints on protein targeting

Björkholm

Harish

Hagström

et al. 2015

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

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“…Several recently published phylogenetic analyses have discussed the origins of the nonmitochondrial ATP/ADP transporters and postulate that the progenitor ATP/ADP translocase protein originated in a chlamydial ancestor and was acquired by the rickettsial ancestor through lateral transfer (6,21,39). Intriguingly, pathogenic chlamydiae (in the family Chlamydiaceae) differ from rickettsiae in that they encode two, not five, Tlc homologues.…”

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confidence: 99%

“…Although rickettsiae and mitochondria are thought to share a common ancestor (6,9,33,41,47,49), there is no significant homology between mitochondrial and nonmitochondrial ATP/ ADP transport proteins (57). This divergence could be linked to the altruistic nature of mitochondria, which provide energy to cells, versus the parasitic nature of rickettsiae.…”

mentioning

confidence: 99%

Study of the Five Rickettsia prowazekii Proteins Annotated as ATP/ADP Translocases (Tlc): Only Tlc1 Transports ATP/ADP, While Tlc4 and Tlc5 Transport Other Ribonucleotides

Audia

Winkler

2006

J Bacteriol

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The obligate intracytoplasmic pathogen Rickettsia prowazekii relies on the transport of many essential compounds from the cytoplasm of the eukaryotic host cell in lieu of de novo synthesis, an evolutionary outcome undoubtedly linked to obligatory growth in this metabolite-replete niche. The paradigm for the study of rickettsial transport systems is the ATP/ADP translocase Tlc1, which exchanges bacterial ADP for host cell ATP as a source of energy, rather than as a source of adenylate. Interestingly, the R. prowazekii genome encodes four open reading frames that are highly homologous to the well-characterized ATP/ADP translocase Tlc1. Therefore, by annotation, the R. prowazekii genome encodes a total of five ATP/ADP translocases: Tlc1, Tlc2, Tlc3, Tlc4, and Tlc5. We have confirmed by quantitative reverse transcriptase PCR that mRNAs corresponding to all five tlc homologues are expressed in R. prowazekii growing in L-929 cells and have shown their heterologous protein expression in Escherichia coli, suggesting that none of the tlc genes are pseudogenes in the process of evolutionary meltdown. However, we demonstrate by heterologous expression in E. coli that only Tlc1 functions as an ATP/ADP transporter. A survey of nucleotides and nucleosides has determined that Tlc4 transports CTP, UTP, and GDP. Intriguingly, although GTP was not transported by Tlc4, it was an inhibitor of CTP and UTP uptake and demonstrated a K i similar to that of GDP. In addition, we demonstrate that Tlc5 transports GTP and GDP. We postulate that Tlc4 and Tlc5 serve the primary function of maintaining intracellular pools of nucleotides for rickettsial nucleic acid biosynthesis and do not provide the cell with nucleoside triphosphates as an energy source, as is the case for Tlc1. Although heterologous expression of Tlc2 and Tlc3 was observed in E. coli, we were unable to identify substrates for these proteins.Rickettsia prowazekii is the etiological agent of epidemic typhus in humans and is designated as a select agent based on its potential use as an agent of bioterrorism. R. prowazekii is an obligate intracellular bacterium and grows only within the cytoplasm of a eukaryotic host cell, unbounded by a host-derived membrane vesicle. As a consequence of growth in this nutrient-rich niche, R. prowazekii has evolved several unique transport systems specific for large, charged metabolites, such as UDP-glucose, S-adenosylmethionine, ATP, NAD, UMP, GMP, and AMP (11,12,45,52,54,55). The ability to transport substrates that are present in the host cell cytosol and rarely available in the extracellular milieu has likely contributed to the evolution of the small-sized rickettsial genome (834 open reading frames [ORFs]); many of the de novo biosynthetic pathways characteristic of free-living bacteria are no longer present in rickettsiae (8). The ATP/ADP translocase Tlc1 is the most thoroughly characterized of these transport systems (1-5, 13, 14, 16, 18, 27, 36, 50, 53, 56). Tlc1 is an obligateexchange transport system that catalyzes the equilibration of...

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“…As non-mitochondrial ATP/ADP translocases (ATP-importing) are distributed in plant chloroplasts, microsporidia and intracellular parasitic bacteria (Rickettsia, Chlamydiaceae), a relatively recent acquisition by microsporidia and plants via independent horizontal gene transfers from bacteria has been hypothesized (Koonin et al 2004, Méténier and). An alternate hypothesis has been proposed in a phylogenetic study supporting a very ancient origin for all mitochondrial and non-mitochondrial ("plastid/parasite") ATP/ADP translocases (Amiri et al 2003). The "plastid/parasite" gene would have been present in a bacterial ancestor of mitochondria and Rickettsia, and then transferred into the nuclear genome of the early eukaryotic cell.…”

Section: Cuniculimentioning

confidence: 99%

Post-genomics of microsporidia, with emphasis on a model of minimal eukaryotic proteome: a review

Texier

Brosson²,

Alaoui³

et al. 2005

FOLIA PARASIT

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Abstract. The genome sequence of the microsporidian parasite Encephalitozoon cuniculi Levaditi, Nicolau et Schoen, 1923 contains about 2,000 genes that are representative of a non-redundant potential proteome composed of 1,909 protein chains. The purpose of this review is to relate some advances in the characterisation of this proteome through bioinformatics and experimental approaches. The reduced diversity of the set of E. cuniculi proteins is perceptible in all the compilations of predicted domains, orthologs, families and superfamilies, available in several public databases. The phyletic patterns of orthologs for seven eukaryotic organisms support an extensive gene loss in the fungal clade, with additional deletions in E. cuniculi. Most microsporidial orthologs are the smallest ones among eukaryotes, justifying an interest in the use of these compacted proteins to better discriminate between essential and non-essential regions. The three components of the E. cuniculi mRNA capping apparatus have been especially well characterized and the three-dimensional structure of the cap methyltransferase has been elucidated following the crystallisation of the microsporidial enzyme Ecm1. So far, our mass spectrometry-based analyses of the E. cuniculi spore proteome has led to the identification of about 170 proteins, one-quarter of these having no clearly predicted function. Immunocytochemical studies are in progress to determine the subcellular localisation of microsporidia-specific proteins. Posttranslational modifications such as phosphorylation and glycosylation are expected to be soon explored.

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Deep Origin of Plastid/Parasite ATP/ADP Translocases

Cited by 55 publications

References 59 publications

Mitochondrial genomes are retained by selective constraints on protein targeting

Mitochondrial genomes are retained by selective constraints on protein targeting

Study of the Five Rickettsia prowazekii Proteins Annotated as ATP/ADP Translocases (Tlc): Only Tlc1 Transports ATP/ADP, While Tlc4 and Tlc5 Transport Other Ribonucleotides

Post-genomics of microsporidia, with emphasis on a model of minimal eukaryotic proteome: a review

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