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The mitochondrial genomes of Euphausia pacifica and Thysanoessa raschii sequenced using 454 next-generation sequencing, with a phylogenetic analysis of their position in the Malacostracan family tree

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Abstract

Euphausiid krill play a critical role in coastal and oceanic food webs, linking primary producers to upper trophic levels. In addition, some species support commercial fisheries worldwide. Despite their ecological importance, the genetics of these important species remain poorly described. To improve our understanding of the genetics of these ecological links, we sequenced the mitochondrial genomes of two species of North Pacific krill, Euphausia pacifica and Thysanoessa raschii, using long-range PCR and 454 GS Junior next-generation sequencing technology. The E. pacifica mitogenome (14,692 + base pairs (bp)) encodes 13 protein-coding genes (PCGs), two ribosomal RNA (rRNA) genes, and at least 22 transfer RNA (tRNA) genes. The T. raschii mitogenome (14,240 + bp) encodes 13 PCGs, two rRNA genes, and at least 19 tRNA genes. The gene order in both species is similar to that of E. superba. Comparisons between Bering Sea and Yellow Sea E. pacifica revealed a total of 644 variable sites. The most variable protein-coding gene were atp8 (7.55 %, 12 of 159 sites variable), nad4 (6.35 %, 85 variable sites) and nad6 (6.32 %, 33 variable sites). Phylogenetic analyses to assess the phylogenetic position of the Euphausiacea, using the concatenated nucleic acid sequences of E. pacifica and T. raschii along with 46 previously published malacostracan mitogenomes, support the monophyly of the order Decapoda and indicate that the Euphausiacea share a common ancestor with the Decapoda. Future research should utilize this sequence data to explore the population genetics and molecular ecology of these species.

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References

  1. Brinton E (1962) The distribution of Pacific euphausiids. Bull Scripps Inst Oceanogr Univ Calif 8:51–269

    Google Scholar 

  2. Mauchline J, Fisher LR (1969) The biology of euphausiids. Adv Mar Biol 7:1–454

    Article  Google Scholar 

  3. Timofeev SF (1993) Distribution and age composition of euphausiids in waters around the Spitsbergen Archipelago. Oceanology 33:105–109

    Google Scholar 

  4. De Pitta C, Bertolucci C, Mazzotta GM, Bernante F, Rizzo G, De Nardi B, Pallavicini A, Lanfranchi G, Costa R (2008) Systematic sequencing of mRNA from the Antarctic krill (Euphausia superba) and first tissue specific transcriptional signature. BMC Genomics 9:45–58

    Article  PubMed  PubMed Central  Google Scholar 

  5. Zane L, Ostellari L, Maccatrozzo L, Battaglia B, Patarnello T (1998) Molecular evidence for genetic subdivision of Antarctic krill (Euphausia superba Dana) populations. Proc Royal Soc B 265:2387–2391

    Article  CAS  Google Scholar 

  6. Goodall-Copestake WP, Pérez-Espona S, Clark MS, Murphy EJ, Seear PJ, Tarling GA (2010) Swarms of diversity at the gene cox1 in Antarctic krill. Heredity 104:513–518

    Article  CAS  PubMed  Google Scholar 

  7. Machida RJ, Masaki UM, Mitsugu MY, Mutsumi N, Nishida S (2004) Organization of the mitochondrial genome of Antarctic Krill Euphausia superba (Crustacea: Malacostraca). Mar Biotechnol 6:238–250. doi:10.1007/s10126-003-0016-6

    Article  CAS  PubMed  Google Scholar 

  8. Shen X, Wang H, Ren J, Tian M, Wang M (2010) The mitochondrial genome of Euphausia superba (Prydz Bay) (Crustacea: Malacostraca: Euphausiacea) reveals a novel gene arrangement and potential molecular markers. Mol Biol Rep 37(2):771–784. doi:10.1007/s11033-009-9602-7

    Article  CAS  PubMed  Google Scholar 

  9. Johansson M, Duda E, Sremba A, Banks M, Peterson W (2012) Assessing population-level variation in the mitochondrial genome of Euphausia superba using 454 next-generation sequencing. Mol Biol Rep 39(5):5755–5760. doi: 10.1007/s11033-011-1385-y

    Google Scholar 

  10. Jarman S, Elliott N, Nicol S, McMinn A, Newman S (1999) The base composition of the krill genome and its potential susceptibility to damage by UV-B. Antarct Sci 11:23–26

    Article  Google Scholar 

  11. Shen X, Wang H, Wang M, Liu B (2011) The complete mitochondrial genome sequence of Euphausia pacifica (Malacostraca: Euphausiacea) reveals a novel gene order and unusual tandem repeats. Genome 54:911–922

    Article  CAS  PubMed  Google Scholar 

  12. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  13. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  14. Cheng S, Chang SY, Gravitt P (1994) Long PCR. Nature 369:684–685. doi:10.1038/369684a0

    Article  CAS  PubMed  Google Scholar 

  15. Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20(17):3252–3255

    Article  CAS  PubMed  Google Scholar 

  16. Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDraw (OGDRAW)—a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52(5–6):267–274

    Article  CAS  PubMed  Google Scholar 

  17. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  19. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  20. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75(5):758–771

    Article  Google Scholar 

  21. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  22. Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinf 10:356

    Article  Google Scholar 

  23. Shen X, Ren J, Cui Z, Sha Z, Wang B, Xiang J, Liu B (2007) The complete mitochondrial genomes of two common shrimps (Litopenaeus vannamei and Fenneropenaeus chinensis) and their phylogenomic considerations. Gene 403(1–2):98–109

    Article  CAS  PubMed  Google Scholar 

  24. De Bruijn MH (1983) Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304(5923):234–241

    Article  PubMed  Google Scholar 

  25. Clary DO, Wolstenholme DR (1983) Genes for cytochrome c oxidase subunit 1, URF2, and three tRNAs in Drosophila mitochondrial DNA. Nucleic Acids Res 11(19):6859–6872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fox TD (1987) Natural variation in the genetic code. Ann Rev Genet 21:67–91

    Article  CAS  PubMed  Google Scholar 

  27. Park DS, Suh SJ, Oh HW, Hebert PD (2010) Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers. BMC Genomics 11:423

    Article  PubMed  PubMed Central  Google Scholar 

  28. Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 590(5806):470–474

    Article  Google Scholar 

  29. Liu Y, Cui Z (2011) Complete mitochondrial genome of the Chinese spiny lobster Panulirus stimpsoni (Crustacea: Decapoda): genome characterization and phylogenetic considerations. Mol Biol Rep 38(1):403–410

    Article  CAS  PubMed  Google Scholar 

  30. Tsang LM, Ma KY, Ahyong ST, Chan T-Y, Chu KH (2008) Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia. Mol Phylogenet Evol 48:359–368

    Article  CAS  PubMed  Google Scholar 

  31. Qian GH, Zhao Q, Wang A, Zhu L, Zhou K, Sun H (2011) Two new decapod (Crustacea, Malacostraca) complete mitochondrial genomes: bearings on the phylogenetic relationships within the Decapoda. Zool J Linn Soc 162(3):471–481

    Article  Google Scholar 

  32. Place AR, Feng X, Steven CR, Fourcade HM, Boore JL (2005) Genetic markers in blue crabs (Callinectes sapidus) II: complete mitochondrial genome sequence and characterization of variation. J Exp Mar Biol Ecol 319(1–2):15–27

    Article  CAS  Google Scholar 

  33. Kilpert F, Podsiadlowski L (2010) The mitochondrial genome of the Japanese skeleton shrimp Caprella mutica (Amphipoda: Caprellidea) reveals a unique gene order and shared apomorphic translocations with Gammaridea. Mitochondrial DNA 21(3–4):77–86

    Article  CAS  PubMed  Google Scholar 

  34. Ito A, Aoki MN, Yokobori S, Wada H (2010) The complete mitochondrial genome of Caprella scaura (Crustacea, Amphipoda, Caprellidea), with emphasis on the unique gene order pattern and duplicated control region. Mitochondrial DNA 21(5):183–190

    Article  CAS  PubMed  Google Scholar 

  35. Liu Y, Cui Z (2010) Complete mitochondrial genome of the Asian paddle crab Charybdis japonica (Crustacea: Decapoda: Portunidae): gene rearrangement of the marine brachyurans and phylogenetic considerations of the decapods. Mol Biol Rep 37(5):2559–2569

    Article  CAS  PubMed  Google Scholar 

  36. Miller AD, Nguyen TT, Burridge CP, Austin CM (2004) Complete mitochondrial DNA sequence of the Australian freshwater crayfish, Cherax destructor (Crustacea: Decapoda: Parastacidae): a novel gene order revealed. Gene 331:65–72

    Article  CAS  PubMed  Google Scholar 

  37. Kilpert F, Podsiadlowski L (2010) The Australian fresh water isopod (Phreatoicidea: Isopoda) allows insights into the early mitogenomic evolution of isopods. Comp Biochem Physiol Part D Genomics Proteomics 5(1):36–44

    Article  PubMed  Google Scholar 

  38. Sun H, Zhou K, Song D (2005) Mitochondrial genome of the Chinese mitten crab Eriocheir japonica sinensis (Brachyura: Thoracotremata: Grapsoidea) reveals a novel gene order and two target regions of gene rearrangements. Gene 349:207–217

    Article  CAS  PubMed  Google Scholar 

  39. Shen X, Sun M, Wu Z, Tian M, Cheng H, Zhao F, Meng X (2009) The complete mitochondrial genome of the ridgetail white prawn Exopalaemon carinicauda Holthuis, 1950 (Crustacean: Decapoda: Palaemonidae) revealed a novel rearrangement of tRNA genes. Gene 437(1–2):1–8

    Article  CAS  PubMed  Google Scholar 

  40. Peregrino-Uriarte AB, Varela-Romero A, Muhlia-Almazan A, Anduro-Corona I, Vega-Heredia S, Gutierrez-Millan LE, De la Rosa-Velez J, Yepiz-Plascencia G (2009) The complete mitochondrial genomes of the yellowleg shrimp Farfantepenaeus californiensis and the blue shrimp Litopenaeus stylirostris (Crustacea: Decapoda. Comp Biochem Physiol Part D Genomics Proteomics 4(1):45–53

    Article  PubMed  Google Scholar 

  41. Yang J-S, Nagasawa H, Fujiwara Y, Tsuchida S, Yang W-J (2010) The complete mitogenome of the hydrothermal vent crab Gandalfus yunohana (Crustacea: Decapoda: Brachyura): a link between the Bythograeoidea and Xanthoidea. Zool Scr 39(6):621–630

    Article  Google Scholar 

  42. Segawa RD, Aotsuka T (2005) The mitochondrial genome of the Japanese freshwater crab, Geothelphusa dehaani (Crustacea: Brachyura): evidence for its evolution via gene duplication. Gene 355:28–39

    Article  CAS  PubMed  Google Scholar 

  43. Ivey JL, Santos SR (2007) The complete mitochondrial genome of the Hawaiian anchialine shrimp Halocaridina rubra Holthuis, 1963 (Crustacea: Decapoda: Atyidae). Gene 394(1–2):35–44

    Article  CAS  PubMed  Google Scholar 

  44. Miller AD, Austin CM (2006) The complete mitochondrial genome of the mantid shrimp Harpiosquilla harpax, and a phylogenetic investigation of the Decapoda using mitochondrial sequences. Mol Phylogenet Evol 38(3):565–574

    Article  CAS  PubMed  Google Scholar 

  45. Kilpert F, Podsiadlowski L (2006) The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features. BMC Genomics 7:241

    Article  PubMed  PubMed Central  Google Scholar 

  46. Miller AD, Murphy NP, Burridge CP, Austin CM (2005) Complete mitochondrial DNA sequences of the decapod crustaceans Pseudocarcinus gigas (Menippidae) and Macrobrachium rosenbergii (Palaemonidae). Mar Biotechnol 7(4):339–349

    Article  CAS  PubMed  Google Scholar 

  47. Yamauchi MM, Miya MU, Machida RJ, Nishida M (2004) PCR-based approach for sequencing mitochondrial genomes of decapod crustaceans, with a practical example from kuruma prawn (Marsupenaeus japonicus). Mar Biotechnol 6(5):419–429

    Article  CAS  PubMed  Google Scholar 

  48. Bauza-Ribot MM, Jaume D, Juan C, Pons J (2009) The complete mitochondrial genome of the subterranean crustacean Metacrangonyx longipes (Amphipoda): a unique gene order and extremely short control region. Mitochondrial DNA 20(4):88–99

    Article  CAS  PubMed  Google Scholar 

  49. Liu Y, Cui Z (2010) The complete mitochondrial genome of the mantid shrimp Oratosquilla oratoria (Crustacea: Malacostraca: Stomatopoda): novel non-coding regions features and phylogenetic implications of the Stomatopoda. Comp Biochem Physiol Part D Genomics Proteomics 5(3):190–198

    Article  CAS  PubMed  Google Scholar 

  50. Hickerson MJ, Cunningham CW (2000) Dramatic mitochondrial gene rearrangements in the hermit crab Pagurus longicarpus (Crustacea, anomura). Mol Biol Evol 17(4):639–644

    Article  CAS  PubMed  Google Scholar 

  51. Yamauchi M, Miya M, Nishida M (2002) Complete mitochondrial DNA sequence of the Japanese spiny lobster, Panulirus japonicus (Crustacea: Decapoda). Gene 295(1):89–96

    Article  CAS  PubMed  Google Scholar 

  52. Wilson K, Cahill V, Ballment E, Benzie J (2000) The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol Biol Evol 17(6):863–874

    Article  CAS  PubMed  Google Scholar 

  53. Yamauchi MM, Miya MU, Nishida M (2003) Complete mitochondrial DNA sequence of the swimming crab, Portunus trituberculatus (Crustacea: Decapoda: Brachyura). Gene 311:129–135

    Article  CAS  PubMed  Google Scholar 

  54. Yang JS, Nagasawa H, Fujiwara Y, Tsuchida S, Yang WJ (2008) The complete mitochondrial genome sequence of the hydrothermal vent galatheid crab Shinkaia crosnieri (Crustacea: Decapoda: Anomura): a novel arrangement and incomplete tRNA suite. BMC Genomics 9:257

    Article  PubMed  PubMed Central  Google Scholar 

  55. Cook CE, Yue Q, Akam M (2005) Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc Biol Sci 272(1569):1295–1304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ki JS, Dahms HU, Hwang JS, Lee JS (2009) The complete mitogenome of the hydrothermal vent crab Xenograpsus testudinatus (Decapoda, Brachyura) and comparison with brachyuran crabs. Comp Biochem Physiol Part D Genomics Proteomics 4(4):290–299

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a NOAA award to CIMRS (Award No. NA06NMF4550286). The authors also gratefully acknowledge O. Drechsel for assistance with constructing genome maps with OGDRAW, B. Slikas, D. Steel, A. Alexander, and D. Jacobson for assistance with 454 sequencing, and T. Shaw, J. Peterson, J. Menkel, and J. Fisher for krill sample collection. The manuscript was greatly improved by the advice of two anonymous reviewers.

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Authors and Affiliations

  1. Cooperative Institute for Marine Resources Studies, Oregon State University, Newport, OR, USA

    Mattias L. Johansson, Angela L. Sremba, Leah R. Feinberg & Michael A. Banks

  2. Coastal Oregon Marine Experiment Station, Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR, USA

    Michael A. Banks

  3. Hatfield Marine Science Center, National Marine Fisheries Service, NOAA, Newport, OR, USA

    William T. Peterson

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  1. Mattias L. Johansson
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  2. Angela L. Sremba
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  3. Leah R. Feinberg
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  4. Michael A. Banks
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  5. William T. Peterson
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Correspondence to Mattias L. Johansson.

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Johansson, M.L., Sremba, A.L., Feinberg, L.R. et al. The mitochondrial genomes of Euphausia pacifica and Thysanoessa raschii sequenced using 454 next-generation sequencing, with a phylogenetic analysis of their position in the Malacostracan family tree. Mol Biol Rep 39, 9009–9021 (2012). https://doi.org/10.1007/s11033-012-1772-z

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