A 5 S rRNA Gene is Present in the Mitochondrial Genome of the ProtistReclinomonas americanabut is Absent from Red Algal Mitochondrial DNA

Lang, B. Franz; Goff, Lynda J.; Gray, Michael W.

doi:10.1006/jmbi.1996.0486

Cited by 29 publications

(19 citation statements)

References 27 publications

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“…Moreover, this RNA is a component of the mitoribosomes of flowering plants, algae, and at least one protist (Lang et al, 1996). Fungal and animal mitoribosomes, however, are not thought to contain this RNA (Curgy, 1985;Bogdanov et al, 1995), even though preparations of nucleic acids from their purified mitochondria generally yield an easily distinguishable species with a size compatible with that of 5S rRNA (Tapper et al, 1983).…”

Section: Discussionmentioning

confidence: 99%

Evidence for the Presence of 5S rRNA in Mammalian Mitochondria

Magalhães

Andreu²,

Schon

1998

MBoC

112

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Mammalian mitochondrial ribosomes contain two prokaryotic-like rRNAs, 12S and 16S, both encoded by mitochondrial DNA. As opposed to cytosolic ribosomes, however, these ribosomes are not thought to contain 5S rRNA. For this reason, it has been unclear whether 5S rRNA, which can be detected in mitochondrial preparations, is an authentic organellar species imported from the cytosol or is merely a copurifying cytosol-derived contaminant. We now show that 5S rRNA is tightly associated with highly purified mitochondrial fractions of human and rat cells and that 5S rRNA transcripts derived from a synthetic gene transfected transiently into human cells are both expressed in vivo and present in highly purified mitochondria and mitoplasts. We conclude that 5S rRNA is imported into mammalian mitochondria, but its function there still remains to be clarified. INTRODUCTIONMitochondria are organelles present in virtually all eukaryotic cells, responsible for most of the energy production required for normal cellular homeostasis. Human mitochondria possess their own DNA (mtDNA), which encodes the two RNA species present in mitochondrial ribosomes (12S and 16S rRNAs), a full set of transfer RNAs (tRNAs) (22 genes) required for protein synthesis (O'Brien et al., 1990), and 13 polypeptides, all constituents of respiratory chain complexes (Anderson et al., 1981).Because mitochondria possess a fully functional genetic apparatus capable of replication, transcription, and translation, they are often considered to be intracellular organelles endowed with a partial autonomy. This autonomy, however, is more apparent than real; in addition to the components encoded by mtDNA, all of the remaining enzymes required for proper functioning of the mitochondrion's genetic machinery (such as DNA and RNA polymerases, ribosomal proteins, aminoacyl tRNA synthetases, etc.) are encoded by nuclear DNA (nDNA), synthesized in the cytosol, and imported into the organelle (Schatz and Dobberstein, 1996;Neupert, 1997). The same is true for all enzymes involved in the myriad metabolic pathways that take place in the mitochondrial environment.Interestingly, at least two mitochondrial enzymes, RNase MRP (a site-specific endoribonuclease involved in primer RNA metabolism in mammalian mitochondria [Chang and Clayton, 1987;Topper and Clayton, 1990;Li et al., 1994]) and RNase P (an endoribonuclease involved in tRNA processing [Doerson et al., 1985]), are ribonucleoproteins that contain an RNA moiety that is encoded by nDNA and is imported into the organelle. However, unlike the mechanisms for protein import into mitochondria, the mechanisms of RNA import into mitochondria are poorly understood.The importation of RNA into mitochondria was first postulated over 30 years ago, as a corollary to mitochondrial protein synthesis and the lack of a full set of tRNA genes in the mitochondrial genome of Tetrahymena (Suyama and Eyer, 1967). This postulate was proven recently (Rusconi and Cech, 1996), and the import of tRNAs into mitochondria has now been (Schneider, 1994;Kaz...

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Section: Discussionmentioning

confidence: 99%

Evidence for the Presence of 5S rRNA in Mammalian Mitochondria

Magalhães

Andreu²,

Schon

1998

MBoC

112

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“…4A). The ms RNA showed similarity (43 out of the 129 nucleotides of the ms RNA) to mt 5S rRNA of P. wickerhamii (Wol et al 1994) and had 32 (shown as asterisks) of the 64 invariant residues (designated by A, U, G, C, R and Y) which were speci®ed by Lang et al (1996). Interestingly, although ms RNA shows only a low level of sequence similarity to other 5S rRNAs reported to date and has a GC content of only 22.5%, the secondary structure constructed using the computer program LRNA (Zucker 1989;Jaeger et al 1989; for the calculation, a temperature of 22°C was selected, because this is the optimal temperature for the growth of D. discoideum) showed the conventional 5S rRNA structure for bacteria with a conserved GAAC sequence in one of the loops (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…2C, and concluded that RNA editing does not occur in this molecule. As the size of ms RNA was very similar to that of 5S rRNAs, the ms RNA sequence was aligned with 5S rRNAs from the mitochondria of wheat (Triticum aestivum, M10361; Spencer et al 1981 Lang et al 1996) and a chlorophycean alga (Prototheca wickerhamii; U02970, Wol et al 1994) (Fig. 4A).…”

Section: Resultsmentioning

confidence: 99%

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Characterization of a novel small RNA encoded by Dictyostelium discoideum mitochondrial DNA

Morio

Urushihara

et al. 1998

Mol Gen Genet

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In this study, we analyzed a mitochondrial small (ms) RNA in Dictyostelium discoideum, which is 129 nucleotides long and has a GC content of only 22.5%. In the mitochondrial DNA, a single-copy gene (msr) for the ms RNA was located downstream of the gene for large-subunit rRNA. The location of msr was similar to that of the 5S rRNA gene in prokaryotes and chloroplasts, but clearly different from that in mitochondria of plants, liverwort and the chlorophycean alga Prototheca wikerhamii, in which small-subunit rRNA and 5S rRNA genes are closely linked. THe primary sequence of ms rRNA showed low homology with mitochondrial 5S rRNA from plants, liverwort and the chlorophycean alga, but the proposed secondary structure of ms RNA was similar to that of cytoplasmic 5S rRNA. In addition, ms RNA showed a highly conserved GAAC sequence in the same loop as in common 5S rRNA. However, ms RNA was detected mainly in the mitochondrial 25,000 x g supernatant fraction which was devoid of ribosomes. It is possible that ms RNA is an evolutionary derivative of mitochondrial 5S rRNA.

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“…Plant mitochondrial ribosomes do contain a distinctive 5S rRNA species (Cunningham et al 1976;Leaver and Harmey 1976;Spencer et al 1981), encoded by the mitochondrial genome (Bonen and Gray 1980;Oda et al 1992;Unseld et al 1997;Kubo et al 2000). A recognizable 5S rRNA gene is also present in some protist mitochondrial genomes, notably those of certain green, red, and brown algae (Wolff et al 1994;Ohta et al 1998;Burger et al 1999;Turmel et al 1999Turmel et al , 2002aTurmel et al , 2000bOudot-Le Secq et al 2001, 2002 and jakobid flagellates (Lang et al 1996. However, an obvious 5S rRNA gene has not been identified in other protist mtDNAs (Gray et al 1998), or in any of the more than 100 animal mitochondrial genomes completely sequenced to date.…”

Section: Introductionmentioning

confidence: 99%

Discovery and characterization of Acanthamoeba castellanii mitochondrial 5S rRNA

Bullerwell

Schnare²,

Gray³

2003

RNA

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Although 5S rRNA is a highly conserved and universal component of eubacterial, archaeal, chloroplast, and eukaryotic cytoplasmic ribosomes, a mitochondrial DNA-encoded 5S rRNA has so far been identified only in land plants and certain protists. This raises the question of whether 5S rRNA is actually required for and used in mitochondrial translation. In the protist Acanthamoeba castellanii, BLAST searches fail to reveal a 5S rRNA gene in the complete mitochondrial genome sequence, nor is a 5S-sized RNA species detectable in ethidium bromide-stained gels of highly purified mitochondrial RNA preparations. Here we show that an alternative visualization technique, UV shadowing, readily detects a novel, mitochondrion-specific small RNA in A. castellanii mitochondrial RNA preparations, and that this RNA species is, in fact, a 5S rRNA encoded by the A. castellanii mitochondrial genome. These results emphasize the need for caution when interpreting negative results that suggest the absence of 5S rRNA and/or a mitochondrial DNA-encoded 5S rRNA sequence in other (particularly protist) mitochondrial systems.

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A 5 S rRNA Gene is Present in the Mitochondrial Genome of the ProtistReclinomonas americanabut is Absent from Red Algal Mitochondrial DNA

Cited by 29 publications

References 27 publications

Evidence for the Presence of 5S rRNA in Mammalian Mitochondria

Evidence for the Presence of 5S rRNA in Mammalian Mitochondria

Characterization of a novel small RNA encoded by Dictyostelium discoideum mitochondrial DNA

Discovery and characterization of Acanthamoeba castellanii mitochondrial 5S rRNA

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