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The mitochondrial genomes of two nemerteans, Cephalothrix sp. (Nemertea: Palaeonemertea) and Paranemertes cf. peregrina (Nemertea: Hoplonemertea)

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Abstract

The mitochondrial genome sequences were determined for two species of nemerteans, Cephalothrix sp. (15,800 bp sequenced, near-complete) and Paranemertes cf. peregrina (14,558 bp, complete). As seen in most metazoans, the genomes encode 13 protein, 2 ribosomal RNA and 22 transfer RNA genes. The nucleotide composition is strongly biased toward A and T, as is typical for metazoan mtDNAs. There is also a significant strand skew in the distribution of these nucleotides, with the coding strand being richer in T than A and in G than C. All genes are transcribed in the same direction except for trnP and trnT, which is consistent with that reported for Cephalothrix hongkongiensis and Lineus viridis. Gene arrangement of Cephalothrix sp. is identical to that of C. hongkongiensis, while in P. cf. peregrina it is similar to L. viridis, but differs significantly from the three Cephalothrix species in the position of four protein-coding genes and seven tRNAs. Some protein-coding genes have 3′ end stem-loop structures, which may allow mRNA processing without flanking tRNAs. The major non-coding regions observed in the two genomes with potential to form stem-loop structures may be involved in the initiation of replication or transcription. The average Ka/Ks values, varying from 0.12 to 0.89, are markedly different among the 13 mitochondrial protein-coding genes, suggesting that there may exist different selective pressure among mitochondrial genes of nemerteans.

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Abbreviations

atp6 and atp8:

ATP synthase subunits 6 and 8

cob :

Cytochrome b

cox13:

Subunits I–III of cytochrome c oxidase

nad16 and nad4L:

NADH dehydrogenase subunits 1–6 and 4L

rrnL and rrnS:

The large and small subunits of ribosomal RNA

trnX :

Transfer RNA molecules with corresponding amino acids denoted by the one-letter code and codon indicated in parentheses (xxx) when necessary

DHU:

Dihydrouridine loop

mtDNA:

Mitochondrial DNA

NC:

Non-coding region

PCR:

Polymerase chain reaction

kb:

Kilobase

bp:

Base pair

R:

A/G

Y:

C/T

W:

A/T

K:

G/T

N:

A/G/C/T

References

  1. Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780

    Article  PubMed  CAS  Google Scholar 

  2. Shadel GS, Clayton DA (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66:409–435. doi:10.1146/annurev.biochem.66.1.409

    Article  PubMed  CAS  Google Scholar 

  3. Boore JL, Brown WM (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 8:668–674. doi:10.1016/S0959-437X(98)80035-X

    Article  PubMed  CAS  Google Scholar 

  4. Boore JL, Macey JR, Medina M (2005) Sequencing and comparing whole mitochondrial genomes of animals. Methods Enzymol 395:311–348. doi:10.1016/S0076-6879(05)95019-2

    Article  PubMed  CAS  Google Scholar 

  5. Kajihara H, Chernyshev AV, Sun SC, Sundberg P, Crandall FB (2008) Checklist of nemertean genera and species published between 1995 and 2007. Spec Diver 13:245–274

    Google Scholar 

  6. Chen HX, Sundberg P, Norenburg JL, Sun SC (2009) The complete mitochondrial genome of Cephalothrix simula (Iwata) (Nemertea: Palaeonemertea). Gene 442:8–17. doi:10.1016/j.gene.2009.04.015

    Article  PubMed  CAS  Google Scholar 

  7. Podsiadlowski L, Braband A, Struck TH, von Döhren J, Bartolomaeus T (2009) Phylogeny and mitochondrial gene order variation in Lophotrochozoa in the light of new mitogenomic data from Nemertea. BMC Genomics 10:364. doi:10.1186/1471-2164-10-364

    Article  PubMed  Google Scholar 

  8. Turbeville JM, Smith DM (2007) The partial mitochondrial genome of the Cephalothrix rufifrons (Nemertea, Palaeonemertea): characterization and implications for the phylogenetic position of Nemertea. Mol Phylogenet Evol 43:1056–1065. doi:10.1016/j.ympev.2006.10.025

    Article  PubMed  CAS  Google Scholar 

  9. Chen HX, Strand M, Norenburg JL, Sun SC, Kajihara H, Chernyshev AV, Maslakova SA, Sundberg P (2010) Statistical parsimony networks and species assemblages in cephalotrichid nemerteans (Nemertea). PLoS ONE 5:e12885. doi:10.1371/journal.pone.0012885

    Article  PubMed  Google Scholar 

  10. Sambrook JRD (2001) Rapid isolation of yeast DNA. In: Sambrook JRD (ed) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, pp 631–632

    Google Scholar 

  11. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  12. Palumbi S (1996) Nucleic acids: II. the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer Associates, Sunderland, pp 205–247

    Google Scholar 

  13. Boore JL, Brown WM (2000) Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol 17:87–106

    PubMed  CAS  Google Scholar 

  14. Hall J (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  15. 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

    Article  PubMed  CAS  Google Scholar 

  16. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  17. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358

    Article  PubMed  CAS  Google Scholar 

  18. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  19. De Rijk P, De Wachter R (1997) RnaViz, a program for the visualisation of RNA secondary structure. Nucleic Acids Res 25:4679–4684

    Article  PubMed  Google Scholar 

  20. Stothard P, Wishart DS (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21:537–539. doi:10.1093/bioinformatics/bti054

    Article  PubMed  CAS  Google Scholar 

  21. Serb JM, Lydeard C (2003) Complete mtDNA sequence of the north American freshwater mussel, Lampsilis ornata (Unionidae): an examination of the evolution and phylogenetic utility of mitochondrial genome organization in Bivalvia (Mollusca). Mol Biol Evol 20:1854–1866. doi:10.1093/molbev/msg218

    Article  PubMed  CAS  Google Scholar 

  22. Boore JL (2006) The complete sequence of the mitochondrial genome of Nautilus macromphalus (Mollusca: Cephalopoda). BMC Genomics 7:182. doi:10.1186/1471-2164-7-182

    Article  PubMed  Google Scholar 

  23. Yokobori SI, Pääbo S (1995) tRNA editing in metazoans. Nature 377:490. doi:10.1038/377490a0

    Article  PubMed  CAS  Google Scholar 

  24. Lavrov DV, Brown WM, Boore JL (2000) A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proc Natl Acad Sci USA 97:13738–13742. doi:10.1073/pnas.250402997

    Article  PubMed  CAS  Google Scholar 

  25. Masta SE, Boore JL (2004) The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol 21:893–902. doi:10.1093/molbev/msh096

    Article  PubMed  CAS  Google Scholar 

  26. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216

    Article  PubMed  CAS  Google Scholar 

  27. Anderson S, Bankier AT, Barrell BG et al (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Article  PubMed  CAS  Google Scholar 

  28. Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474

    Article  PubMed  CAS  Google Scholar 

  29. Ojala D, Merkel C, Gelfand R, Attardi G (1980) The tRNA genes punctuate the reading of genetic information in human mitochondrial DNA. Cell 22:393–403. doi:10.1016/0092-8674(80)90350-5

    Article  PubMed  CAS  Google Scholar 

  30. Montoya J, Gaines GL, Attardi G (1983) The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell 34:151–159. doi:10.1016/0092-8674(83)90145-9

    Article  PubMed  CAS  Google Scholar 

  31. Boore JL, Brown WM (1994) Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138:423–443

    PubMed  CAS  Google Scholar 

  32. Kim I, Lee EM, Seol KY, Yun EY, Lee YB, Hwang JS, Jin BR (2006) The mitochondrial genome of the Korean hairstreak, Coreana raphaelis (Lepidoptera: Lycaenidae). Insect Mol Biol 15:217–225. doi:10.1111/j.1365-2583.2006.00630.x

    Article  PubMed  CAS  Google Scholar 

  33. Fenn JD, Cameron SL, Whiting MF (2007) The complete mitochondrial genome sequence of the Mormon cricket (Anabrus simplex: Tettigoniidae: Orthoptera) and an analysis of control region variability. Insect Mol Biol 16:239–252. doi:10.1111/j.1365-2583.2006.00721.x

    Article  PubMed  CAS  Google Scholar 

  34. Jermiin LS, Graur D, Lowe RM, Crozier RH (1994) Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes. J Mol Evol 39:160–173

    PubMed  CAS  Google Scholar 

  35. Francino MP, Ochman H (1997) Strand asymmetries in DNA evolution. Trends Genet 13:240–245. doi:10.1016/S0168-9525(97)01118-9

    Article  PubMed  CAS  Google Scholar 

  36. Hassanin A, Leger N, Deutsch J (2005) Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of metazoa, and consequences for phylogenetic inferences. Syst Biol 54:277–298

    Article  PubMed  Google Scholar 

  37. Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271

    Article  PubMed  CAS  Google Scholar 

  38. Boore JL, Brown WM (1995) Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics 141:305–319

    PubMed  CAS  Google Scholar 

  39. Ikemura T (1982) Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J Mol Biol 158:573–597. doi:10.1016/0022-2836(82)90250-9

    Article  PubMed  CAS  Google Scholar 

  40. Sharp PM, Matassi G (1994) Codon usage and genome evolution. Curr Opin Genet Dev 4:851–860

    Article  PubMed  CAS  Google Scholar 

  41. Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA 96:4482–4487

    Article  PubMed  CAS  Google Scholar 

  42. Helfenbein KG, Brown WM, Boore JL (2001) The complete mitochondrial genome of the articulate brachiopod Terebratalia transversa. Mol Biol Evol 18:1734–1744

    PubMed  CAS  Google Scholar 

  43. Broughton RE, Reneau PC (2006) Spatial covariation of mutation and nonsynonymous substitution rates in vertebrate mitochondrial genomes. Mol Biol Evol 23:1516–1524. doi:10.1093/molbev/msl013

    Article  PubMed  CAS  Google Scholar 

  44. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503

    Article  PubMed  Google Scholar 

  45. Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18:486–487

    Article  PubMed  Google Scholar 

  46. Li W (1997) Rates and patterns of nucleotide substitution. In: Andrew DS (ed) Molecular evolution. Sinauer Associates, Sunderland, pp 177–210

    Google Scholar 

  47. Macey JR, Larson A, Ananjeva NB, Papenfuss TJ (1997) Replication slippage may cause parallel evolution in the secondary structures of mitochondrial transfer RNAs. Mol Biol Evol 14:30–39

    PubMed  CAS  Google Scholar 

  48. Yamazaki N, Ueshima R, Terrett JA et al (1997) Evolution of pulmonate gastropod mitochondrial genomes: comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics 145:749–758

    PubMed  CAS  Google Scholar 

  49. Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498

    PubMed  CAS  Google Scholar 

  50. Yokobori S, Pääbo S (1997) Polyadenylation creates the discriminator nucleotide of chicken mitochondrial tRNA(Tyr). J Mol Biol 265:95–99

    Article  PubMed  CAS  Google Scholar 

  51. Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217. doi:10.1016/0022-2836(88)90452-4

    Article  PubMed  CAS  Google Scholar 

  52. Boyce TM, Zwick ME, Aquadro CF (1989) Mitochondrial DNA in the bark weevils: size, structure and heteroplasmy. Genetics 123:825–836

    PubMed  CAS  Google Scholar 

  53. L’Abbe D, Duhaime JF, Lang BF, Morais R (1991) The transcription of DNA in chicken mitochondria initiates from one major bidirectional promoter. J Biol Chem 266:10844–10850

    PubMed  Google Scholar 

  54. Kolpakov R, Bana G, Kucherov G (2003) mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res 31:3672–3678

    Article  PubMed  CAS  Google Scholar 

  55. Curole JP, Kocher TD (1999) Mitogenomics: digging deeper with complete mitochondrial genomes. Trends Ecol Evol 14:394–398

    Article  PubMed  Google Scholar 

  56. Moritz C, Brown WM (1987) Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA 84:7183–7187

    Article  PubMed  CAS  Google Scholar 

  57. Stanton DJ, Daehler LL, Moritz CC, Brown WM (1994) Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA. Genetics 137:233–241

    PubMed  CAS  Google Scholar 

  58. Saccone C, De Giorgi C, Gissi C, Pesole G, Reyes A (1999) Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene 238:195–209. doi:10.1016/S0378-1119(99)00270-X

    Article  PubMed  CAS  Google Scholar 

  59. Vallès Y, Boore JL (2006) Lophotrochozoan mitochondrial genomes. Integr Comp Biol 46:544–557. doi:10.1093/Icb/Icj056

    Article  PubMed  Google Scholar 

  60. Shen X, Ma X, Ren J, Zhao F (2009) A close phylogenetic relationship between Sipuncula and Annelida evidenced from the complete mitochondrial genome sequence of Phascolosoma esculenta. BMC Genomics 10:136. doi:10.1186/1471-2164-10-136

    Article  PubMed  Google Scholar 

  61. Noguchi Y, Endo K, Tajima F, Ueshima R (2000) The mitochondrial genome of the brachiopod Laqueus rubellus. Genetics 155:245–259

    PubMed  CAS  Google Scholar 

  62. Nakao M, Sako Y, Ito A (2003) The mitochondrial genome of the tapeworm Taenia solium: a finding of the abbreviated stop codon. U J Parasitol 89:633–635

    Article  CAS  Google Scholar 

  63. Plaisance L, Huyse T, Littlewood DT, Bakke TA, Bachmann L (2007) The complete mitochondrial DNA sequence of the monogenean Gyrodactylus thymalli (Platyhelminthes: Monogenea), a parasite of grayling (Thymallus thymallus). Mol Biochem Parasitol 154:190–194. doi:10.1016/j.molbiopara.2007.04.012

    Article  PubMed  CAS  Google Scholar 

  64. Steinauer ML, Nickol BB, Broughton R, Orti G (2005) First sequenced mitochondrial genome from the phylum Acanthocephala (Leptorhynchoides thecatus) and its phylogenetic position within Metazoa. J Mol Evol 60:706–715. doi:10.1007/s00239-004-0159-8

    Article  PubMed  CAS  Google Scholar 

  65. Min GS, Park JK (2009) Eurotatorian paraphyly: revisiting phylogenetic relationships based on the complete mitochondrial genome sequence of Rotaria rotatoria (Bdelloidea: Rotifera: Syndermata). BMC Genomics 10:533. doi:10.1186/1471-2164-10-533

    Article  PubMed  Google Scholar 

  66. Fearnley IM, Walker JE (1986) Two overlapping genes in bovine mitochondrial DNA encode membrane components of ATP synthase. EMBO J 5:2003–2008

    PubMed  CAS  Google Scholar 

  67. Dunn CW, Hejnol A, Matus DQ et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749. doi:10.1038/nature06614

    Article  PubMed  CAS  Google Scholar 

  68. Struck TH, Fisse F (2008) Phylogenetic position of Nemertea derived from phylogenomic data. Mol Biol Evol 25:728–736. doi:10.1093/molbev/msn019

    Article  PubMed  CAS  Google Scholar 

  69. Rawlings TA, Collins TM, Bieler R (2001) A major mitochondrial gene rearrangement among closely related species. Mol Biol Evol 18:1604–1609

    PubMed  CAS  Google Scholar 

  70. Morrison CL, Harvey AW, Lavery S, Tieu K, Huang Y, Cunningham CW (2002) Mitochondrial gene rearrangements confirm the parallel evolution of the crab-like form. Proc R Soc Lond B 269:345–350. doi:10.1098/rspb.2001.1886

    Article  CAS  Google Scholar 

  71. Lavrov DV, Brown WM, Boore JL (2004) Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proc R Soc Lond B 271:537–544. doi:10.1098/rspb.2003.2631

    Article  Google Scholar 

  72. Akasaki T, Nikaido M, Tsuchiya K, Segawa S, Hasegawa M, Okada N (2006) Extensive mitochondrial gene arrangements in coleoid Cephalopoda and their phylogenetic implications. Mol Phylogenet Evol 38:648–658. doi:10.1016/j.ympev.2005.10.018

    Article  PubMed  CAS  Google Scholar 

  73. Faure E, Casanova JP (2006) Comparison of chaetognath mitochondrial genomes and phylogenetical implications. Mitochondrion 6:258–262. doi:10.1016/j.mito.2006.07.004

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (30970333) and the Swedish Research Council (80565801) (to PS). We are grateful to Wei Shi and Dong-Li Xu for assisting with the analyses.

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Chen, HX., Sundberg, P., Wu, HY. et al. The mitochondrial genomes of two nemerteans, Cephalothrix sp. (Nemertea: Palaeonemertea) and Paranemertes cf. peregrina (Nemertea: Hoplonemertea). Mol Biol Rep 38, 4509–4525 (2011). https://doi.org/10.1007/s11033-010-0582-4

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