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The Oxytricha trifallax mitochondrial genome.

Swart EC, Nowacki M, Shum J, Stiles H, Higgins BP, Doak TG, Schotanus K, Magrini VJ, Minx P, Mardis ER, Landweber LF - Genome Biol Evol (2011)

Bottom Line: This region on the chromosome is also close to the end of the most terminal member of a series of duplications, hinting at a possible association between the plasmid and the duplications.The presence of mitochondrial telomeres on the mitochondrial plasmid suggests that such plasmids may be a vehicle for lateral transfer of telomeric sequences between mitochondrial genomes.We conjecture that the extreme divergence observed in ciliate mitochondrial genomes may be due, in part, to repeated invasions by relatively error-prone DNA polymerase-bearing mobile elements.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, USA.

ABSTRACT
The Oxytricha trifallax mitochondrial genome contains the largest sequenced ciliate mitochondrial chromosome (~70 kb) plus a ~5-kb linear plasmid bearing mitochondrial telomeres. We identify two new ciliate split genes (rps3 and nad2) as well as four new mitochondrial genes (ribosomal small subunit protein genes: rps- 2, 7, 8, 10), previously undetected in ciliates due to their extreme divergence. The increased size of the Oxytricha mitochondrial genome relative to other ciliates is primarily a consequence of terminal expansions, rather than the retention of ancestral mitochondrial genes. Successive segmental duplications, visible in one of the two Oxytricha mitochondrial subterminal regions, appear to have contributed to the genome expansion. Consistent with pseudogene formation and decay, the subtermini possess shorter, more loosely packed open reading frames than the remainder of the genome. The mitochondrial plasmid shares a 251-bp region with 82% identity to the mitochondrial chromosome, suggesting that it most likely integrated into the chromosome at least once. This region on the chromosome is also close to the end of the most terminal member of a series of duplications, hinting at a possible association between the plasmid and the duplications. The presence of mitochondrial telomeres on the mitochondrial plasmid suggests that such plasmids may be a vehicle for lateral transfer of telomeric sequences between mitochondrial genomes. We conjecture that the extreme divergence observed in ciliate mitochondrial genomes may be due, in part, to repeated invasions by relatively error-prone DNA polymerase-bearing mobile elements.

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rps3 genes in ciliate mitochondrial genomes (Euplotes minuta—GQ903130; Tetrahymena pyriformis—AF160864; Paramecium aurelia—NC_001324). The rps3_a and rps3_b multiple sequence alignments are indicated above and below a schematic representation of the split rps3 genes. Regions with substantial sequence similarity are indicated in dark purple, whereas those that are poorly conserved are indicated in pink; the rps3_a and rps3_b parts are on distant loci. The rps3 extension annotated as a part of this gene in Euplotes does not align to any of the other rps3 sequences. Multiple sequence alignments were generated with Muscle (Edgar 2004) with default parameters.
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fig2: rps3 genes in ciliate mitochondrial genomes (Euplotes minuta—GQ903130; Tetrahymena pyriformis—AF160864; Paramecium aurelia—NC_001324). The rps3_a and rps3_b multiple sequence alignments are indicated above and below a schematic representation of the split rps3 genes. Regions with substantial sequence similarity are indicated in dark purple, whereas those that are poorly conserved are indicated in pink; the rps3_a and rps3_b parts are on distant loci. The rps3 extension annotated as a part of this gene in Euplotes does not align to any of the other rps3 sequences. Multiple sequence alignments were generated with Muscle (Edgar 2004) with default parameters.

Mentions: The Euplotesrps3 is unusually long (767 and 768 amino acids for E. minuta and Euplotescrassus, respectively) in comparison to the rps3 orthologues found in the Oxytricha (∼349 aa), Tetrahymena (330 aa), and Paramecium (234 aa) and was show to contain the C-terminal domain of rps3 in the 5′-terminal half of this gene (de Graaf et al. 2009) (fig. 2). The 3′ half of the Euplotes gene has no detectable similarity to rps3. In Oxytricha, this same gene is divided into a shorter, 5′-terminal portion containing the C-terminal rps3 domain, followed by a longer portion of unknown function. We identified an Oxytricha homolog to a gene previously classified as rps3 (Burger et al. 2000) in Tetrahymena and Paramecium but disputed as such (Brunk et al. 2003). As for Tetrahymena and Paramecium and unlike Euplotes (de Graaf et al. 2009), HHpred predicts with high probability (5.1 × 10-06 for Oxytricha) that an N-terminal rps3 domain is present in the mitochondrial genome, in an ORF that we label rps3_a. It is possible that the rps3 N-terminal domain is encoded in a missing portion of the Euplotes mitochondrial genome. It therefore appears that this is another split gene present in most, if not all, sequenced ciliate mitochondrial genomes. Accordingly, the previously disputed rps3 (N-terminal) can now be called rps3_a, and the recently classified C-terminal rps3 portion, rps3_b, consistent with the split gene nomenclature in Burger et al. (2000).


The Oxytricha trifallax mitochondrial genome.

Swart EC, Nowacki M, Shum J, Stiles H, Higgins BP, Doak TG, Schotanus K, Magrini VJ, Minx P, Mardis ER, Landweber LF - Genome Biol Evol (2011)

rps3 genes in ciliate mitochondrial genomes (Euplotes minuta—GQ903130; Tetrahymena pyriformis—AF160864; Paramecium aurelia—NC_001324). The rps3_a and rps3_b multiple sequence alignments are indicated above and below a schematic representation of the split rps3 genes. Regions with substantial sequence similarity are indicated in dark purple, whereas those that are poorly conserved are indicated in pink; the rps3_a and rps3_b parts are on distant loci. The rps3 extension annotated as a part of this gene in Euplotes does not align to any of the other rps3 sequences. Multiple sequence alignments were generated with Muscle (Edgar 2004) with default parameters.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3318907&req=5

fig2: rps3 genes in ciliate mitochondrial genomes (Euplotes minuta—GQ903130; Tetrahymena pyriformis—AF160864; Paramecium aurelia—NC_001324). The rps3_a and rps3_b multiple sequence alignments are indicated above and below a schematic representation of the split rps3 genes. Regions with substantial sequence similarity are indicated in dark purple, whereas those that are poorly conserved are indicated in pink; the rps3_a and rps3_b parts are on distant loci. The rps3 extension annotated as a part of this gene in Euplotes does not align to any of the other rps3 sequences. Multiple sequence alignments were generated with Muscle (Edgar 2004) with default parameters.
Mentions: The Euplotesrps3 is unusually long (767 and 768 amino acids for E. minuta and Euplotescrassus, respectively) in comparison to the rps3 orthologues found in the Oxytricha (∼349 aa), Tetrahymena (330 aa), and Paramecium (234 aa) and was show to contain the C-terminal domain of rps3 in the 5′-terminal half of this gene (de Graaf et al. 2009) (fig. 2). The 3′ half of the Euplotes gene has no detectable similarity to rps3. In Oxytricha, this same gene is divided into a shorter, 5′-terminal portion containing the C-terminal rps3 domain, followed by a longer portion of unknown function. We identified an Oxytricha homolog to a gene previously classified as rps3 (Burger et al. 2000) in Tetrahymena and Paramecium but disputed as such (Brunk et al. 2003). As for Tetrahymena and Paramecium and unlike Euplotes (de Graaf et al. 2009), HHpred predicts with high probability (5.1 × 10-06 for Oxytricha) that an N-terminal rps3 domain is present in the mitochondrial genome, in an ORF that we label rps3_a. It is possible that the rps3 N-terminal domain is encoded in a missing portion of the Euplotes mitochondrial genome. It therefore appears that this is another split gene present in most, if not all, sequenced ciliate mitochondrial genomes. Accordingly, the previously disputed rps3 (N-terminal) can now be called rps3_a, and the recently classified C-terminal rps3 portion, rps3_b, consistent with the split gene nomenclature in Burger et al. (2000).

Bottom Line: This region on the chromosome is also close to the end of the most terminal member of a series of duplications, hinting at a possible association between the plasmid and the duplications.The presence of mitochondrial telomeres on the mitochondrial plasmid suggests that such plasmids may be a vehicle for lateral transfer of telomeric sequences between mitochondrial genomes.We conjecture that the extreme divergence observed in ciliate mitochondrial genomes may be due, in part, to repeated invasions by relatively error-prone DNA polymerase-bearing mobile elements.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, USA.

ABSTRACT
The Oxytricha trifallax mitochondrial genome contains the largest sequenced ciliate mitochondrial chromosome (~70 kb) plus a ~5-kb linear plasmid bearing mitochondrial telomeres. We identify two new ciliate split genes (rps3 and nad2) as well as four new mitochondrial genes (ribosomal small subunit protein genes: rps- 2, 7, 8, 10), previously undetected in ciliates due to their extreme divergence. The increased size of the Oxytricha mitochondrial genome relative to other ciliates is primarily a consequence of terminal expansions, rather than the retention of ancestral mitochondrial genes. Successive segmental duplications, visible in one of the two Oxytricha mitochondrial subterminal regions, appear to have contributed to the genome expansion. Consistent with pseudogene formation and decay, the subtermini possess shorter, more loosely packed open reading frames than the remainder of the genome. The mitochondrial plasmid shares a 251-bp region with 82% identity to the mitochondrial chromosome, suggesting that it most likely integrated into the chromosome at least once. This region on the chromosome is also close to the end of the most terminal member of a series of duplications, hinting at a possible association between the plasmid and the duplications. The presence of mitochondrial telomeres on the mitochondrial plasmid suggests that such plasmids may be a vehicle for lateral transfer of telomeric sequences between mitochondrial genomes. We conjecture that the extreme divergence observed in ciliate mitochondrial genomes may be due, in part, to repeated invasions by relatively error-prone DNA polymerase-bearing mobile elements.

Show MeSH
Related in: MedlinePlus