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: 1.21). 08/2011; 22(4):130-42. DOI: 10.3109/19401736.2011.624611
Source: PubMed


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.

Download full-text


Available from: Dennis V. Lavrov, Mar 27, 2014
  • Source
    • "Throughout the work, care was taken to use sterilized tools and containers , and gloves were worn. The genetic classification was done by matching DNA sequences to global and local data to achieve the most accurate species identification for the sampled specimens (Bayha et al. 2010;Pett et al. 2011). We designed DNA primers (Table 1) for the locally found jellyfish. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The species of Aequorea attract much scientific interest as they contain the unique Green Fluorescent Protein (GFP). In this work we describe for the first time the discovery of a hydrozoan jellyfish belonging to the genus Aequorea from the Israeli eastern Mediterranean that contains and exhibits fluorescent protein. Finding Aequorea macrodactyla (Brandt, 1835) in the eastern Mediterranean indicates that changes are occurring in the gelatinous fauna of this area. This hydromedusa is known in the seas adjoining the Mediterranean though most of its records are more than four decades old. We examined and identified the newly discovered Israeli Aequorea species by combining two phylogenetic systems, traditional morphological phylogeny and molecular phylogenetics. The molecular identification determined that the species is A. macrodactyla but with minor genetic differences in the mtDNA 16S gene marker. A 1% difference between the Israeli and the Japanese A. macrodactyla was demonstrated, which suggests that the genetic difference between the Israeli and the Japanese population is small but existent. Invasive pathways for this jellyfish were examined by phylogenetic and taxonomic relationships with similar Cnidaria. The results indicate introduction from the Indo-Pacific as invasive pathway, probably by human transportation, and the discovery of A. macrodactyla in the eastern Mediterranean Sea could be interpreted as part of the changes in marine biota as a result of cumulative effects of anthropogenic and global changes that affect the eastern Mediterranean basin.
    Full-text · Article · Jul 2015
  • Source
    • "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! "
    [Show abstract] [Hide abstract]
    ABSTRACT: Recent phylogenetic analyses resulting from collection of whole genome data suggest that ctenophores, or comb jellies, are sister to all other animals. Even before publication, this result prompted discussion among researchers. Here, I counter common criticisms raised about this result and show that assumptions placing sponges as the basal-most extant animal lineage are based on limited evidence and questionable premises. For example, the idea that sponges are simple and the reported similarity of sponge choanocytes to Choanflagellata do not provide useful characters for determining the positions of sponges within the animal tree. Intertwined with discussion of basal metazoan phylogeny is consideration of the evolution of neuronal systems. Recent data show that neural systems of ctenophores are vastly different from those of other animals and use different sets of cellular and genetic mechanisms. Thus, neural systems appear to have at least two independent origins regardless of whether ctenophores or sponges are the earliest branching extant animal lineage. © 2015. Published by The Company of Biologists Ltd.
    Full-text · Article · Feb 2015 · Journal of Experimental Biology
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Quinol oxidation in the catalytic Qo site of cytochrome (cyt) bc1 complexes is the key step of the Q cycle mechanism which laid the ground for Mitchell's chemiosmotic theory of energy conversion. Bifurcated electron transfer upon quinol oxidation enables proton uptake and release on opposite membrane sides thus generating a proton gradient that fuels ATP synthesis in cellular respiration and photosynthesis. The Qo site architecture formed by cyt b and Rieske iron-sulfur protein (ISP) impedes harmful bypass reactions. Catalytic importance is assigned to four residues of cyt b formerly described as PEWY motif in the context of mitochondrial complexes, which we now denominate Qo motif as comprehensive evolutionary sequence analysis of cyt b shows substantial natural variance of the motif with phylogenetically-specific patterns. In particular, the Qo motif is identified as PEWY in mitochondria, α- and ε-Proteobacteria, Aquificae, Chlorobi, Cyanobacteria, and chloroplasts. PDWY is present in Gram-positive bacteria, Deinococcus-Thermus and haloarchaea, and PVWY in β- and γ-Proteobacteria. PPWF only exists in Archaea. Distinct patterns for acidophilic organisms indicate environment-specific adaptations. Importantly, the presence of PDWY and PEWY is correlated with the redox potential of Rieske ISP and quinone species. We propose that during evolution from low to high potential electron-transfer systems in the emerging oxygenic atmosphere, cyt bc1 complexes with PEWY as Qo motif prevailed to efficiently use high potential ubiquinone as substrate, whereas cyt b with PDWY operate best with low potential Rieske ISP and menaquinone, with the latter being the likely composition of the ancestral cyt bc1 complex.
    Full-text · Article · Jul 2014 · Genome Biology and Evolution
Show more