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Group II introns break new boundaries: presence in a bilaterian's genome.

Vallès Y, Halanych KM, Boore JL - PLoS ONE (2008)

Bottom Line: Here we report the first group II intron found in the mitochondrial genome of a bilaterian worm.This intron is found in the mtDNA of an annelid worm, (an undescribed species of Nephtys), where the complete sequence revealed a 1819 bp group II intron inside the cox1 gene.We infer that this intron is the result of a recent horizontal gene transfer event from a viral or bacterial vector into the mitochondrial genome of Nephtys sp.

View Article: PubMed Central - PubMed

Affiliation: Department of Energy (DOE), Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, California, USA.

ABSTRACT
Group II introns are ribozymes, removing themselves from their primary transcripts, as well as mobile genetic elements, transposing via an RNA intermediate, and are thought to be the ancestors of spliceosomal introns. Although common in bacteria and most eukaryotic organelles, they have never been reported in any bilaterian animal genome, organellar or nuclear. Here we report the first group II intron found in the mitochondrial genome of a bilaterian worm. This location is especially surprising, since animal mitochondrial genomes are generally distinct from those of plants, fungi, and protists by being small and compact, and so are viewed as being highly streamlined, perhaps as a result of strong selective pressures for fast replication while establishing germ plasm during early development. This intron is found in the mtDNA of an annelid worm, (an undescribed species of Nephtys), where the complete sequence revealed a 1819 bp group II intron inside the cox1 gene. We infer that this intron is the result of a recent horizontal gene transfer event from a viral or bacterial vector into the mitochondrial genome of Nephtys sp. Our findings hold implications for understanding mechanisms, constraints, and selective pressures that account for patterns of animal mitochondrial genome evolution.

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Predicted secondary structure of the Nephtys sp. group II intron.Potentially conserved secondary structure consisting of a central core from which radiate six domains (I–VI). The RT and partial maturase ORF are encoded within domain IV. EBS and IBS indicate sites where interaction between the intron and exon (respectively) occurs when splicing. Greek symbols designate sequence sites potentially involved in tertiary structure.
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pone-0001488-g001: Predicted secondary structure of the Nephtys sp. group II intron.Potentially conserved secondary structure consisting of a central core from which radiate six domains (I–VI). The RT and partial maturase ORF are encoded within domain IV. EBS and IBS indicate sites where interaction between the intron and exon (respectively) occurs when splicing. Greek symbols designate sequence sites potentially involved in tertiary structure.

Mentions: We have determined the complete sequence of the mitochondrial genome of Nephtys sp., a carnivorous polychaete inhabiting the intertidal and subtidal zones. This genome is typical of animal mtDNAs in possessing 37 genes on a single circular molecule with few and short non-coding regions [17]. However, contrary to all expectations, the protein coding gene cox1 contains a group II intron (Fig. 1). We confirmed that the intron is a part of the mtDNA rather than a nuclear pseudogene by using polymerase chain reactions (PCR) to amplify the entire mtDNA in two overlapping pieces using inverted primers that anneal within the intron (Table 2). We verified that this intron is, in fact, removed from the mRNA by cloning and sequencing cDNA made from the transcripts of the cox1 gene. We identified it as a group II self-splicing intron by a detailed examination of its sequence and potential secondary structure that revealed these diagnostic features: (1) conserved GUGYG and AY nucleotides at the 5′ and 3′ intron boundaries, respectively; (2) conserved sequence of domain V, which is the catalytic core of the intron's ribozymic activity; (3) presence of an ORF for a contiguous reverse transcriptase (RT) gene and a partial maturase gene; (4) potential secondary structure with six helical domains radiating from a central core consistent with the highly conserved secondary structure of group II introns (Fig. 1) [2], [6], [19], [20]. This is the first case of any intron found in the mtDNA of any bilaterian animal (Table 1).


Group II introns break new boundaries: presence in a bilaterian's genome.

Vallès Y, Halanych KM, Boore JL - PLoS ONE (2008)

Predicted secondary structure of the Nephtys sp. group II intron.Potentially conserved secondary structure consisting of a central core from which radiate six domains (I–VI). The RT and partial maturase ORF are encoded within domain IV. EBS and IBS indicate sites where interaction between the intron and exon (respectively) occurs when splicing. Greek symbols designate sequence sites potentially involved in tertiary structure.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2198948&req=5

pone-0001488-g001: Predicted secondary structure of the Nephtys sp. group II intron.Potentially conserved secondary structure consisting of a central core from which radiate six domains (I–VI). The RT and partial maturase ORF are encoded within domain IV. EBS and IBS indicate sites where interaction between the intron and exon (respectively) occurs when splicing. Greek symbols designate sequence sites potentially involved in tertiary structure.
Mentions: We have determined the complete sequence of the mitochondrial genome of Nephtys sp., a carnivorous polychaete inhabiting the intertidal and subtidal zones. This genome is typical of animal mtDNAs in possessing 37 genes on a single circular molecule with few and short non-coding regions [17]. However, contrary to all expectations, the protein coding gene cox1 contains a group II intron (Fig. 1). We confirmed that the intron is a part of the mtDNA rather than a nuclear pseudogene by using polymerase chain reactions (PCR) to amplify the entire mtDNA in two overlapping pieces using inverted primers that anneal within the intron (Table 2). We verified that this intron is, in fact, removed from the mRNA by cloning and sequencing cDNA made from the transcripts of the cox1 gene. We identified it as a group II self-splicing intron by a detailed examination of its sequence and potential secondary structure that revealed these diagnostic features: (1) conserved GUGYG and AY nucleotides at the 5′ and 3′ intron boundaries, respectively; (2) conserved sequence of domain V, which is the catalytic core of the intron's ribozymic activity; (3) presence of an ORF for a contiguous reverse transcriptase (RT) gene and a partial maturase gene; (4) potential secondary structure with six helical domains radiating from a central core consistent with the highly conserved secondary structure of group II introns (Fig. 1) [2], [6], [19], [20]. This is the first case of any intron found in the mtDNA of any bilaterian animal (Table 1).

Bottom Line: Here we report the first group II intron found in the mitochondrial genome of a bilaterian worm.This intron is found in the mtDNA of an annelid worm, (an undescribed species of Nephtys), where the complete sequence revealed a 1819 bp group II intron inside the cox1 gene.We infer that this intron is the result of a recent horizontal gene transfer event from a viral or bacterial vector into the mitochondrial genome of Nephtys sp.

View Article: PubMed Central - PubMed

Affiliation: Department of Energy (DOE), Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, California, USA.

ABSTRACT
Group II introns are ribozymes, removing themselves from their primary transcripts, as well as mobile genetic elements, transposing via an RNA intermediate, and are thought to be the ancestors of spliceosomal introns. Although common in bacteria and most eukaryotic organelles, they have never been reported in any bilaterian animal genome, organellar or nuclear. Here we report the first group II intron found in the mitochondrial genome of a bilaterian worm. This location is especially surprising, since animal mitochondrial genomes are generally distinct from those of plants, fungi, and protists by being small and compact, and so are viewed as being highly streamlined, perhaps as a result of strong selective pressures for fast replication while establishing germ plasm during early development. This intron is found in the mtDNA of an annelid worm, (an undescribed species of Nephtys), where the complete sequence revealed a 1819 bp group II intron inside the cox1 gene. We infer that this intron is the result of a recent horizontal gene transfer event from a viral or bacterial vector into the mitochondrial genome of Nephtys sp. Our findings hold implications for understanding mechanisms, constraints, and selective pressures that account for patterns of animal mitochondrial genome evolution.

Show MeSH