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
    • "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.
    Journal of Experimental Biology 02/2015; 218(Pt 4):592-597. DOI:10.1242/jeb.111872 · 2.90 Impact Factor
  • 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.
    Genome Biology and Evolution 07/2014; 6(7). DOI:10.1093/gbe/evu147 · 4.23 Impact Factor
    • "We here argue that no convincing evidence to exclude Ctenophora from Epitheliozoa has been presented thus far, because topologies in which ctenophores branch off first from the metazoan tree are very likely to be artifactual (Pick et al. 2010; Philippe et al. 2011; Nosenko et al. 2013). Certainly, the highly anticipated publication of comprehensive analyses of ctenophoran nuclear genomes will shed more light on this issue (see e.g., Byrum 2012; Maxmen 2013; Pennisi 2013), but it can be expected that these genomes are highly unusual, as has already been shown for ctenophoran mt genomes (Pett et al. 2011; Kohn et al. 2012). Thus, one should be careful to avoid circular reasoning by interpreting genomic features such as lack of certain genes (e.g., those coding for the microRNA processing machinery) (Maxwell et al. 2012) as ancestral characters in support of the pre-conceived ''Ctenophora-first'' hypothesis—comb jellies appear anatomically highly derived, so this is likely to be true for their genomes as well. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Understanding how important phenotypic, developmental, and genomic features of animals originated and evolved is essential for many fields of biological research, but such understanding depends on robust hypotheses about the phylogenetic interrelationships of the higher taxa to which the studied species belong. Molecular approaches to phylogenetics have proven able to revolutionize our knowledge of organismal evolution. However, with respect to the deepest splits in the metazoan Tree of Life-the relationships between Bilateria and the four non-bilaterian phyla (Porifera, Placozoa, Ctenophora, and Cnidaria)-no consensus has been reached yet, since a number of different, often contradictory, hypotheses with sometimes spectacular implications have been proposed in recent years. Here, we review the recent literature on the topic and contrast it with more classical perceptions based on analyses of morphological characters. We conclude that the time is not yet ripe to rewrite zoological textbooks and advocate a conservative approach when it comes to developing scenarios of the early evolution of animals.
    Integrative and Comparative Biology 03/2013; 53(3). DOI:10.1093/icb/ict008 · 2.93 Impact Factor
Show more