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Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: Insight from mtDNA and the nuclear genome - PubMed

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Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: Insight from mtDNA and the nuclear genome

Walker Pett et al. Mitochondrial DNA. 2011 Aug.

Abstract

Recent advances in sequencing technology have led to a rapid accumulation of mitochondrial DNA (mtDNA) sequences, which now represent the wide spectrum of animal diversity. However, one animal phylum--Ctenophora--has, to date, remained completely unsampled. Ctenophores, a small group of marine animals, are of interest due to their unusual biology, controversial phylogenetic position, and devastating impact as invasive species. Using data from the Mnemiopsis leidyi genome sequencing project, we Polymerase Chain Reaction (PCR) amplified and analyzed its complete mitochondrial (mt-) genome. At just over 10 kb, the mt-genome of M. leidyi is the smallest animal mtDNA ever reported and is among the most derived. It has lost at least 25 genes, including atp6 and all tRNA genes. We show that atp6 has been relocated to the nuclear genome and has acquired introns and a mitochondrial targeting presequence, while tRNA genes have been genuinely lost, along with nuclear-encoded mt-aminoacyl tRNA synthetases. The mt-genome of M. leidyi also displays extremely high rates of sequence evolution, which likely led to the degeneration of both protein and rRNA genes. In particular, encoded rRNA molecules possess little similarity with their homologs in other organisms and have highly reduced secondary structures. At the same time, nuclear encoded mt-ribosomal proteins have undergone expansions, likely to compensate for the reductions in mt-rRNA. The unusual features identified in M. leidyi mtDNA make this organism an interesting system for the study of various aspects of mitochondrial biology, particularly protein and tRNA import and mt-ribosome structures, and add to its value as an emerging model species. Furthermore, the fast-evolving M. leidyi mtDNA should be a convenient molecular marker for species- and population-level studies.

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Figures

Figure 1
Figure 1. Mitochondrial genome map of Mnemiopsis leidyi

Inferred protein and rRNA genes are indicated by black arrows pointing in the direction of their transcriptional orientation; regions of overlap between them are indicated in red. The blue shaded area between two internal circles indicates AT-richness of the genome, with the inner circle corresponding to 0 %AT and the other circle – to 100 %AT. The genome encodes genes for subunits 1–5 of NADH dehydrogenase (nad1–5), subunits 1–3 of cytochrome c oxidase (cox1–3), cytochrome b (cob), the large and small subunits of mt-ribosomal RNA (rnl and rns), and two genes of low-homology to other mitochondrial proteins putatively assigned as nad4L and nad6.

Figure 2
Figure 2. Comparison of atp9 sequences in M. leidyi and other animals

Multiple sequence alignment of atp9 from Amphimedon queenslandica (A.q.), Nematostella vectensis (N.v.), Mnemiopsis leidyi (M.l.), Trichoplax adhaerens (T.a.), Homo sapiens (H.s.), and the consensus sequence from all mt-genomes available on the NCBI organellar genome resources website (mt) were created with MAFFT6 (Katoh and Toh, 2008). Presequence cleavage sites as predicted by TargetP are indicated with filled triangles, intron positions are indicated with open triangles, and the conserved motif in the presequence is marked by a rectangle.

Figure 3
Figure 3. Conserved secondary structures in M. leidyi mt-rRNAs

Predicted secondary structures in small (A) and large subunit (B) rRNAs inferred by both manual inspection and Infernal alignments. Helices in srRNA are numbered as in in Brimacombe (1995); those in lrRNA – as in Leffers et al. (1987). Conserved nucleotide positions referenced in the text are indicated with arrows.

Figure 4
Figure 4. Phylogenetic analysis of animal relationships using mitochondrial sequence data

Posterior majority-rule consensus tree obtained from the analysis of concatenated mitochondrial amino acid sequences inferred from the five genes best-conserved in Mnemiopsis (cob, cox1–3, and nad5; 1402 aa in total). We used the CAT+F+Γ model in PhyloBayes and ran four independent chains for ~20,000 generations sampling every 10th tree after the first 1000 burnin cycles. The convergence among the chains was monitored with the maxdiff statistics and the analysis was terminated after maxdiff became less than 0.15. The number at each node represents the Bayesian posterior probability.

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References

    1. Alfonzo JD, et al. C to U editing of the anticodon of imported mitochondrial tRNA(Trp) allows decoding of the UGA stop codon in Leishmania tarentolae. The EMBO journal. 1999;18:7056–7062. - PMC - PubMed
    1. Altschul SF, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research. 1997;25:3389–3402. - PMC - PubMed
    1. Avise JC. Molecular Markers, Natural History, and Evolution. Sinauer Associates; Sunderland, MA: 2004.
    1. Ax P. Multicellular animals: a new approach to the phylogenetic order in nature. Springer; Berlin: 1996.
    1. Baker LD, Reeve MR. Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity. Marine biology. 1974;26:57–62.

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