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The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: evidence for programmed translational frameshifting.

Rosengarten RD, Sperling EA, Moreno MA, Leys SP, Dellaporta SL - BMC Genomics (2008)

Bottom Line: Here we determined the first complete mitochondrial genome of a hexactinellid sponge, Aphrocallistes vastus, and compared it to published poriferan mtDNAs to further describe characteristics specific to hexactinellid and other sponge mitochondrial genomes.The A. vastus mtDNA consisted of a 17,427 base pair circular molecule containing thirteen protein-coding genes, divergent large and small subunit ribosomal RNAs, and a reduced set of 18 tRNAs.Analysis of the mtDNA of A. vastus has provided evidence diagnostic for +1 programmed translational frameshifting, a phenomenon disparately reported throughout the animal kingdom, but present in the hexactinellid mtDNAs that have been sequenced to date.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520-8104, USA. rafael.rosengarten@yale.edu

ABSTRACT

Background: Mitochondrial genomes (mtDNA) of numerous sponges have been sequenced as part of an ongoing effort to resolve the class-level phylogeny of the Porifera, as well as to place the various lower metazoan groups on the animal-kingdom tree. Most recently, the partial mtDNA of two glass sponges, class Hexactinellida, were reported. While previous phylogenetic estimations based on these data remain uncertain due to insufficient taxon sampling and accelerated rates of evolution, the mtDNA molecules themselves reveal interesting traits that may be unique to hexactinellids. Here we determined the first complete mitochondrial genome of a hexactinellid sponge, Aphrocallistes vastus, and compared it to published poriferan mtDNAs to further describe characteristics specific to hexactinellid and other sponge mitochondrial genomes.

Results: The A. vastus mtDNA consisted of a 17,427 base pair circular molecule containing thirteen protein-coding genes, divergent large and small subunit ribosomal RNAs, and a reduced set of 18 tRNAs. The A. vastus mtDNA showed a typical hexactinellid nucleotide composition and shared a large synteny with the other sequenced glass sponge mtDNAs. It also contained an unidentified open reading frame and large intergenic space region. Two frameshifts, in the cox3 and nad6 genes, were not corrected by RNA editing, but rather possessed identical shift sites marked by the extremely rare tryptophan codon (UGG) followed by the common glycine codon (GGA) in the +1 frame.

Conclusion: Hexactinellid mtDNAs have shown similar trends in gene content, nucleotide composition, and codon usage, and have retained a large gene syntenty. Analysis of the mtDNA of A. vastus has provided evidence diagnostic for +1 programmed translational frameshifting, a phenomenon disparately reported throughout the animal kingdom, but present in the hexactinellid mtDNAs that have been sequenced to date.

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Linearized genomes of all sequenced poriferan mtDNAs. Side-by-side comparison of the mtDNAs of A. vastus and the previously published hexactinellid sponge mtDNAs reveal a large syntenic gene block: atp6-cox3-nad2-nad5-trnF-trnC-nad1-trn(L, I, N, Y)-cob. Variable gene arrangements among the hexactinellids include, but are not limited to, the order of cox2-rnl, the transposition of nad3, and the presence and location of nad6. Demosponges (excepting the homoscleromorph O. carmela) retain the syntenic block cox2-atp8-atp6-cox3 which is highly conserved throughout much of the animal kingdom, while the hexactinellids have lost atp8 and translocated cox2.
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Figure 2: Linearized genomes of all sequenced poriferan mtDNAs. Side-by-side comparison of the mtDNAs of A. vastus and the previously published hexactinellid sponge mtDNAs reveal a large syntenic gene block: atp6-cox3-nad2-nad5-trnF-trnC-nad1-trn(L, I, N, Y)-cob. Variable gene arrangements among the hexactinellids include, but are not limited to, the order of cox2-rnl, the transposition of nad3, and the presence and location of nad6. Demosponges (excepting the homoscleromorph O. carmela) retain the syntenic block cox2-atp8-atp6-cox3 which is highly conserved throughout much of the animal kingdom, while the hexactinellids have lost atp8 and translocated cox2.

Mentions: The complete mitochondrial genome of Aphrocallistes vastus was sequenced and shown to be a 17,427 base pair circular molecule encoding 13 proteins, 2 ribosomal RNA subunits, and 18 tRNAs [Genbank: EU000309] (Figure 1, Table 1). All genes were found to be coded on the same strand. The protein coding genes included 12 of the respiratory genes (atp6, cob, cox1-3, nad1-4, 4L, 5, 6) common to most animal mtDNA, as well as the ATP synthase F0 subunit9 (atp9) found in all published sponge mitochondrial genomes except for Amphimedon [13-16,19]. A 411 bp open reading frame (orf411) of unknown identity and function was located adjacent to the largest, 568 bp, intergenic space (is568), just downstream of the nad4 + trnH + nad6 + trnG genes (Figures 1 and 2). orf411 does not display significant nucleotide or amino acid similarity to either of the unknown ORFs in the I. panicea mtDNA. is568 contains numerous direct repeats and may comprise a control region that includes the origin of replication. A putative control region was inferred in the mitochondrial genome of Amphimedon as well [13].


The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: evidence for programmed translational frameshifting.

Rosengarten RD, Sperling EA, Moreno MA, Leys SP, Dellaporta SL - BMC Genomics (2008)

Linearized genomes of all sequenced poriferan mtDNAs. Side-by-side comparison of the mtDNAs of A. vastus and the previously published hexactinellid sponge mtDNAs reveal a large syntenic gene block: atp6-cox3-nad2-nad5-trnF-trnC-nad1-trn(L, I, N, Y)-cob. Variable gene arrangements among the hexactinellids include, but are not limited to, the order of cox2-rnl, the transposition of nad3, and the presence and location of nad6. Demosponges (excepting the homoscleromorph O. carmela) retain the syntenic block cox2-atp8-atp6-cox3 which is highly conserved throughout much of the animal kingdom, while the hexactinellids have lost atp8 and translocated cox2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2267718&req=5

Figure 2: Linearized genomes of all sequenced poriferan mtDNAs. Side-by-side comparison of the mtDNAs of A. vastus and the previously published hexactinellid sponge mtDNAs reveal a large syntenic gene block: atp6-cox3-nad2-nad5-trnF-trnC-nad1-trn(L, I, N, Y)-cob. Variable gene arrangements among the hexactinellids include, but are not limited to, the order of cox2-rnl, the transposition of nad3, and the presence and location of nad6. Demosponges (excepting the homoscleromorph O. carmela) retain the syntenic block cox2-atp8-atp6-cox3 which is highly conserved throughout much of the animal kingdom, while the hexactinellids have lost atp8 and translocated cox2.
Mentions: The complete mitochondrial genome of Aphrocallistes vastus was sequenced and shown to be a 17,427 base pair circular molecule encoding 13 proteins, 2 ribosomal RNA subunits, and 18 tRNAs [Genbank: EU000309] (Figure 1, Table 1). All genes were found to be coded on the same strand. The protein coding genes included 12 of the respiratory genes (atp6, cob, cox1-3, nad1-4, 4L, 5, 6) common to most animal mtDNA, as well as the ATP synthase F0 subunit9 (atp9) found in all published sponge mitochondrial genomes except for Amphimedon [13-16,19]. A 411 bp open reading frame (orf411) of unknown identity and function was located adjacent to the largest, 568 bp, intergenic space (is568), just downstream of the nad4 + trnH + nad6 + trnG genes (Figures 1 and 2). orf411 does not display significant nucleotide or amino acid similarity to either of the unknown ORFs in the I. panicea mtDNA. is568 contains numerous direct repeats and may comprise a control region that includes the origin of replication. A putative control region was inferred in the mitochondrial genome of Amphimedon as well [13].

Bottom Line: Here we determined the first complete mitochondrial genome of a hexactinellid sponge, Aphrocallistes vastus, and compared it to published poriferan mtDNAs to further describe characteristics specific to hexactinellid and other sponge mitochondrial genomes.The A. vastus mtDNA consisted of a 17,427 base pair circular molecule containing thirteen protein-coding genes, divergent large and small subunit ribosomal RNAs, and a reduced set of 18 tRNAs.Analysis of the mtDNA of A. vastus has provided evidence diagnostic for +1 programmed translational frameshifting, a phenomenon disparately reported throughout the animal kingdom, but present in the hexactinellid mtDNAs that have been sequenced to date.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520-8104, USA. rafael.rosengarten@yale.edu

ABSTRACT

Background: Mitochondrial genomes (mtDNA) of numerous sponges have been sequenced as part of an ongoing effort to resolve the class-level phylogeny of the Porifera, as well as to place the various lower metazoan groups on the animal-kingdom tree. Most recently, the partial mtDNA of two glass sponges, class Hexactinellida, were reported. While previous phylogenetic estimations based on these data remain uncertain due to insufficient taxon sampling and accelerated rates of evolution, the mtDNA molecules themselves reveal interesting traits that may be unique to hexactinellids. Here we determined the first complete mitochondrial genome of a hexactinellid sponge, Aphrocallistes vastus, and compared it to published poriferan mtDNAs to further describe characteristics specific to hexactinellid and other sponge mitochondrial genomes.

Results: The A. vastus mtDNA consisted of a 17,427 base pair circular molecule containing thirteen protein-coding genes, divergent large and small subunit ribosomal RNAs, and a reduced set of 18 tRNAs. The A. vastus mtDNA showed a typical hexactinellid nucleotide composition and shared a large synteny with the other sequenced glass sponge mtDNAs. It also contained an unidentified open reading frame and large intergenic space region. Two frameshifts, in the cox3 and nad6 genes, were not corrected by RNA editing, but rather possessed identical shift sites marked by the extremely rare tryptophan codon (UGG) followed by the common glycine codon (GGA) in the +1 frame.

Conclusion: Hexactinellid mtDNAs have shown similar trends in gene content, nucleotide composition, and codon usage, and have retained a large gene syntenty. Analysis of the mtDNA of A. vastus has provided evidence diagnostic for +1 programmed translational frameshifting, a phenomenon disparately reported throughout the animal kingdom, but present in the hexactinellid mtDNAs that have been sequenced to date.

Show MeSH
Related in: MedlinePlus