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

Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50010, USA.
Mitochondrial DNA (Impact Factor: 1.7). 08/2011; 22(4):130-42. DOI: 10.3109/19401736.2011.624611
Source: PubMed

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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    • "ATPase 9 and extra tRNAs), some sponges have a slightly larger mtDNA genome (approaching 20 kb) (Lavrov et al., 2005) and some cnidarians have linear mtDNA genomes (Bridge et al., 1992). Ctenophores, however, also have a highly divergent mtDNA genome ~11 kb in length and missing several genes – most tRNAs are absent (Pett et al., 2011; The ctenophore lineage is older than sponges? That cannot be right! "
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    • "Interestingly, their mitochondrial genomes are highly divergent in respect to other eukaryotes (Pett et al. 2011; Kohn et al. 2012), therefore we regard these two sequences as the only two exceptions among mitochondrial cyt b. Cyt b 6 f complexes from Cyanobacteria and chloroplasts also carry PEWY and no single exception with aspartate at the second position of the Q o motif was found in this study. "
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