Publication Cover
Mitochondrial DNA
The Journal of DNA Mapping, Sequencing, and Analysis
Volume 22, 2011 - Issue 4
727
Views
65
CrossRef citations to date
0
Altmetric
Full Length Research Paper

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

, , , , , & show all
Pages 130-142 | Received 30 Jun 2011, Accepted 01 Aug 2011, Published online: 10 Oct 2011

References

  • Alfonzo JD, Blanc V, Estevez AM, Rubio MA, Simpson L. 1999. C to U editing of the anticodon of imported mitochondrial tRNA(Trp) allows decoding of the UGA stop codon in rLeishmania tarentolae. EMBO J. 18:7056–7062.
  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402.
  • Avise JC. 2004. Molecular Markers, Natural History, and Evolution. Sunderland, MA: Sinauer Associates.
  • Ax P. 1996. Multicellular animals: a new approach to the phylogenetic order in nature. Berlin: Springer.
  • Baker LD, Reeve MR. 1974. Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity. Mar Biol. 26:57–62.
  • Bokov K, Steinberg SV. 2009. A hierarchical model for evolution of 23S ribosomal RNA. Nature. 457:977–980.
  • Brimacombe R. 1995. The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur J Biochem. 230:365–383.
  • Burger G, Zhu Y, Littlejohn TG, Greenwood SJ, Schnare MN, Lang BF, Gray MW. 2000. Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J Mol Biol. 297:365–380.
  • Burger G, Lavrov DV, Forget L, Lang BF. 2007. Sequencing complete mitochondrial and plastid genomes. Nat Protoc. 2:603–614.
  • Cavalier-Smith T. 1993. Kingdom protozoa and its 18 phyla. Microbiol Mol Biol Rev. 57:953.
  • Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 10:195–205.
  • Charlesworth D, Wright SI. 2001. Breeding systems and genome evolution. Curr Opin Genet Dev. 11:685–690.
  • Chen JY, Schopf JW, Bottjer DJ, Zhang CY, Kudryavtsev AB, Tripathi AB, Wang XQ, Yang YH, Gao X, Yang Y. 2007. Raman spectra of a Lower Cambrian ctenophore embryo from southwestern Shaanxi. China. Proc Natl Acad Sci U S A. 104:6289–6292.
  • Chiusano ML, Alvarez-Valin F, Di Giulio M, D'Onofrio G, Ammirato G, Colonna G, Bernardi G. 2000. Second codon positions of genes and the secondary structures of proteins. Relationships and implications for the origin of the genetic code. Gene. 261:63–69.
  • Colin SP, Costello JH, Hansson LJ, Titelman J, Dabiri JO. 2010. Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi. Proc Natl Acad Sci U S A. 107:17223–17227.
  • Collins AG. 1998. Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc Natl Acad Sci U S A. 95:15458–15463.
  • Crisp MD, Cook LG. 2005. Do early branching lineages signify ancestral traits?. Trends Ecol Evol. 20:122–128.
  • de la Cruz VF, Lake JA, Simpson AM, Simpson L. A minimal ribosomal RNA: sequence and secondary structure of the 9S kinetoplast ribosomal RNA from Leishmania tarentolae. Proc Natl Acad Sci U S A. 1985a; 82:1401–1405.
  • de la Cruz VF, Simpson AM, Lake JA, Simpson L. Primary sequence and partial secondary structure of the 12S kinetoplast (mitochondrial) ribosomal RNA from Leishmania tarentolae: conservation of peptidyl-transferase structural elements. Nucleic Acids Res. 1985b; 13:2337–2356.
  • De Rijk P, Wuyts J, De Wachter R. 2003. RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics. 19:299–300.
  • Denovan-Wright EM, Nedelcu AM, Lee RW. 1998. Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol. 36:285–295.
  • Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 452:745–749.
  • Dzik J. 2002. Possible ctenophoran affinities of the Precambrian “sea-pen” Rangea. J Morphol. 252:315–334.
  • Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc. 2:953–971.
  • Erpenbeck D, Voigt O, Adamski M, Adamska M, Hooper J, Worheide G, Degnan B. 2007. Mitochondrial Diversity of Early-Branching Metazoa Is Revealed by the Complete mt Genome of a Haplosclerid Demosponge. Mol Biol Evol. 24:19–22.
  • Ewing B, Green P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8:186–194.
  • Ewing B, Hillier L, Wendl MC, Green P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175–185.
  • Figueroa-Martinez F, Vazquez-Acevedo M, Cortes-Hernandez P, Garcia-Trejo JJ, Davidson E, King MP, Gonzalez-Halphen D. 2011. What limits the allotopic expression of nucleus-encoded mitochondrial genes? The case of the chimeric Cox3 and Atp6 genes. Mitochondrion. 11:147–154.
  • Frey TG, Mannella CA. 2000. The internal structure of mitochondria. Trends Biochem Sci. 25:319–324.
  • Funes S, Davidson E, Claros MG, van Lis R, Perez-Martinez X, Vazquez-Acevedo M, King MP, Gonzalez-Halphen D. 2002. The typically mitochondrial DNA-encoded ATP6 subunit of the F1F0-ATPase is encoded by a nuclear gene in Chlamydomonas reinhardtii. J Biol Chem. 277:6051–6058.
  • Gillespie JH. 2001. Is the population size of a species relevant to its evolution?. Evolution Int J Org Evolution. 55:2161–2169.
  • Glotz C, Zwieb C, Brimacombe R, Edwards K, Kössel H. 1981. Secondary structure of the large subunit ribosomal RNA from Escherichia coli, Zea mays chloroplast, and human and mouse mitochondrial ribosomes. Nucleic Acids Res. 9:3287–3306.
  • Glover KE, Spencer DF, Gray MW. 2001. Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem. 276:639–648.
  • Gray MW, Lang BF, Burger G. 2004. Mitochondria of protists. Annu Rev Genet. 38:477–524.
  • Graziewicz MA, Longley MJ, Copeland WC. 2006. DNA polymerase gamma in mitochondrial DNA replication and repair. Chem Rev. 106:383–405.
  • Haeckel E. 1866. Generelle Morphologie der Organismen: allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin reformirte Descendenz-Theorie. Berlin: G. Reimer.
  • Haen KM, Lang BF, Pomponi SA, Lavrov DV. 2007. Glass Sponges and Bilaterian Animals Share Derived Mitochondrial Genomic Features: A Common Ancestry or Parallel Evolution?. Mol Biol Evol. 24:1518–1527.
  • Haen KM, Pett W, Lavrov DV. 2010. Parallel loss of nuclear-encoded mitochondrial aminoacyl-tRNA synthetases and mtDNA-encoded tRNAs in Cnidaria. Mol Biol Evol. 27:2216–2219.
  • Hancock L, Goff L, Lane C. 2010. Red algae lose key mitochondrial genes in response to becoming parasitic. Genome Biol Evol. 2:897–910.
  • Harbison GR. 1985. On the classification and evolution of the Ctenophora. In: Conway Morris S, George JD, Gibson R, Platt HM. editors. The origins and relationships of lower invertebrates. Oxford: Clarendon Press78–100.
  • Hazkani-Covo E. 2009. Mitochondrial insertions into primate nuclear genomes suggest the use of numts as a tool for phylogeny. Mol Biol Evol. 26:2175–2179.
  • Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Muller WE, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW. 2009. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci. 276:4261–4270.
  • Helfenbein KG, Fourcade HM, Vanjani RG, Boore JL. 2004. The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes. Proc Natl Acad Sci U S A. 101:10639–10643.
  • Hernandez-Nicaise ML. 1991. Ctenophora. In: Harrison FW, Westfall JA. editors. Placozoa, Porifera, Cnidaria, and Ctenophora. New York, NY: Wiley-Liss, IncVolume 2359–418.
  • Hoffmann RJ, Boore JL, Brown WM. 1992. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics. 131:397–412.
  • Horridge GA. 1964. The giant mitochondria of ctenophore comb plates. QJ micr Sci. 105:301–310.
  • Hyman LH. 1940. The Invertebrates: Protoza Through Ctenophora. New York: McGraw-Hill.
  • Iannelli F, Griggio F, Pesole G, Gissi C. 2007. The mitochondrial genome of Phallusia mammillata and Phallusia fumigata (Tunicata, Ascidiacea): high genome plasticity at intra-genus level. BMC Evol Biol. 7:155.
  • Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9:286–298.
  • Kayal E, Lavrov DV. 2008. The mitochondrial genome of Hydra oligactis (Cnidaria, Hydrozoa) sheds new light on animal mtDNA evolution and cnidarian phylogeny. Gene. 410:177–186.
  • Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 305:567–580.
  • Lang A. 1882. Der Bau von Gunda segmentata und die Verwandtschaft der Plathelminthen mit Coelenteraten und Hirudineen. Mittheilungen aus der Zoologischen Station zu Neapel. zugleich ein Repertorium für Mittelmeerkunde. 3:187–251.
  • Lang BF, Gray MW, Burger G. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet. 33:351–397.
  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics. 23:2947–2948.
  • Lartillot N, Philippe H. 2004. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol. 21:1095–1109.
  • Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 25:2286–2288.
  • Laslett D, Canback B. 2008. ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics. 24:172–175.
  • Lavrov DV. 2011. Key transitions in animal evolution: a mitochondrial DNA perspective. In: Desalle R, Schierwater B. editors. Key transitions in animal evolution. Enfield, NH: Science Publishers35–54.
  • Le TH, Blair D, McManus DP. 2002. Mitochondrial genomes of parasitic flatworms. Trends Parasitol. 18:206–213.
  • Leffers H, Kjems J, Ostergaard L, Larsen N, Garrett RA. 1987. Evolutionary relationships amongst archaebacteria. A comparative study of 23 S ribosomal RNAs of a sulphur-dependent extreme thermophile, an extreme halophile and a thermophilic methanogen. J Mol Biol. 195:43–61.
  • Liu SL, Zhuang Y, Zhang P, Adams KL. 2009. Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus. Mol Biol Evol. 26:875–891.
  • Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955–964.
  • Löytynoja A, Milinkovitch MC. 2001. SOAP, cleaning multiple alignments from unstable blocks. Bioinformatics. 17:573–574.
  • Lynch M, Blanchard JL. 1998. Deleterious mutation accumulation in organelle genomes. Genetica. 102-103:29–39.
  • Lynch M, Koskella B, Schaack S. 2006. Mutation pressure and the evolution of organelle genomic architecture. Science. 311:1727–1730.
  • Manfredi G, Fu J, Ojaimi J, Sadlock JE, Kwong JQ, Guy J, Schon EA. 2002. Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat Genet. 30:394–399.
  • Martin W, Stoebe B, Goremykin V, Hapsmann S, Hasegawa M, Kowallik KV. 1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. 393:162–165.
  • Martindale MQ. 1987. Larval reproduction in the ctenophore Mnemiopsis mccradyi (order Lobata). Mar Biol. 94:409–414.
  • Nawrocki EP, Kolbe DL, Eddy SR. 2009. Infernal 1.0: inference of RNA alignments. Bioinformatics. 25:1335–1337.
  • Ogle JM, Carter AP, Ramakrishnan V. 2003. Insights into the decoding mechanism from recent ribosome structures. Trends Biochem Sci. 28:259–266.
  • Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR. 1992. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics. 130:471–498.
  • Pang K, Martindale MQ. 2008a. Comb jellies (ctenophora): a model for Basal metazoan evolution and development CSH Protoc, doi:10.1101/pdb.emo106.
  • Pang K, Martindale MQ. Ctenophores. Curr Biol. 2008b; 18:R1119–R1120.
  • Pang K, Ryan JF, Mullikin JC, Baxevanis AD, Martindale MQ. 2010. Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. Evodevo. 1:10.
  • Papillon D, Perez Y, Caubit X, Le Parco Y. 2004. Identification of chaetognaths as protostomes is supported by the analysis of their mitochondrial genome. Mol Biol Evol. 21:2122–2129.
  • Pearson WR. 1994. Using the FASTA program to search protein and DNA sequence databases. Methods Mol Biol. 25:365–389.
  • Perna NT, Kocher TD. 1995. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol. 41:353–358.
  • Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Queinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Worheide G, Manuel M. 2009. Phylogenomics revives traditional views on deep animal relationships. Curr Biol. 19:706–712.
  • Pianka ND. 1974. Ctenophora. In: Giese AC, Pearse JS, editors. Reproduction of marine invertebrates. volume 1: Acoelomate and Pseudocoelomate Metazoans New York, NY: Academic Press Inc. p 201–265.
  • Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alie A, Morgenstern B, Manuel M, Worheide G. 2010. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol. 27:1983–1983.
  • Podar M, Haddock SH, Sogin ML, Harbison GR. 2001. A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. Mol Phylogenet Evol. 21:218–230.
  • Polacek N, Mankin AS. 2005. The ribosomal peptidyl transferase center: structure, function, evolution, inhibition. Crit Rev Biochem Mol Biol. 40:285–311.
  • Purcell JE, Shiganova TA, Decker MB, Houde ED. 2001. The ctenophore Mnemiopsis in native and exotic habitats: US estuaries versus the Black Sea basin. Hydrobiologia. 451:145–176.
  • Ratnasingham S, Hebert PD. 2007. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org) Mol Ecol Notes 7., p 355–364.
  • Reitzel AM, Pang K, Ryan JF, Mullikin JC, Martindale MQ, Baxevanis AD, Tarrant AM. 2011. Nuclear receptors from the ctenophore Mnemiopsis leidyi lack a zinc-finger DNA-binding domain: lineage-specific loss or ancestral condition in the emergence of the nuclear receptor superfamily?. Evodevo. 2:3.
  • Ryan JF, Pang K, Mullikin JC, Martindale MQ, Baxevanis AD. 2010. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. Evodevo. 1:9.
  • Schneider A. 2001. Unique aspects of mitochondrial biogenesis in trypanosomatids. Int J Parasitol. 31:1403–1415.
  • Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK. 2003. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell. 115:97–108.
  • Sharma MR, Booth TM, Simpson L, Maslov DA, Agrawal RK. 2009. Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci U S A. 106:9637–9642.
  • Shiganova T, Mirzoyan Z, Studenikina E, Volovik S, Siokou-Frangou I, Zervoudaki S, Christou E, Skirta A, Dumont H. 2001. Population development of the invader ctenophore Mnemiopsis leidyi, in the Black Sea and in other seas of the Mediterranean basin. Mar Biol. 139:431–445.
  • Signorovitch AY, Buss LW, Dellaporta SL. 2007. Comparative Genomics of Large Mitochondria in Placozoans. PLoS Genet. 3:e13.
  • Slamovits CH, Saldarriaga JF, Larocque A, Keeling PJ. 2007. The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both apicomplexan and dinoflagellate mitochondrial genomes. J Mol Biol. 372:356–368.
  • Smits P, Smeitink JA, van den Heuvel LP, Huynen MA, Ettema TJ. 2007. Reconstructing the evolution of the mitochondrial ribosomal proteome. Nucleic Acids Res. 35:4686–4703.
  • Staden R. 1996. The Staden sequence analysis package. Mol Biotechnol. 5:233–241.
  • Stothard P, Wishart DS. 2005. Circular genome visualization and exploration using CGView. Bioinformatics. 21:537–539.
  • Suzuki T, Terasaki M, Takemoto-Hori C, Hanada T, Ueda T, Wada A, Watanabe K. 2001. Structural compensation for the deficit of rRNA with proteins in the mammalian mitochondrial ribosome. Systematic analysis of protein components of the large ribosomal subunit from mammalian mitochondria. J Biol Chem. 276:21724–21736.
  • Wainright PO, Hinkle G, Sogin ML, Stickel SK. 1993. Monophyletic origins of the metazoa: an evolutionary link with fungi. Science. 260:340–342.
  • Wallberg A, Thollesson M, Farris JS, Jondelius U. 2004. The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling. Cladistics. 20:558–578.
  • Wang X, Lavrov DV. 2008. Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE. 3:e2723.
  • Wilson RJ, Williamson DH. 1997. Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev. 61:1–16.
  • Yokobori S, Pääbo S. 1997. Polyadenylation creates the discriminator nucleotide of chicken mitochondrial tRNA(Tyr). J Mol Biol. 265:95–99.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.