Advertisement

Polar Biology

, Volume 37, Issue 8, pp 1133–1144 | Cite as

Transcriptome information of the Arctic green sea urchin and its use in environmental monitoring

  • Jae-Sung Rhee
  • Bo-Mi Kim
  • Beom-Soon Choi
  • Ik-Young Choi
  • Hyun Park
  • In-Young Ahn
  • Jae-Seong Lee
Original Paper

Abstract

The Arctic sea urchin Strongylocentrotus droebachiensis is considered to be a potential indicator species for assessing aquatic environmental conditions in the polar region. To develop a gene resource for the Arctic sea urchin, we sequenced S. droebachiensis cDNAs using a GS-20 sequencer and obtained expressed sequence tags information. In the assembly stage, 31,526 transcripts were obtained and showed a 32 % hit rate in the GenBank non-redundant database with 9,995 unigenes. Of the transcripts obtained in this species, we found several stress- and cellular defense-related genes (antioxidant-related genes and genes from the heat shock protein family) that are useful for the monitoring of pollutant-triggered stress responses at the molecular level. To validate the usefulness of these potential biomarker genes, we analyzed the transcript profiles of selected genes in response to polychlorinated biphenyls (PCB) mixtures (Aroclor 1254) for 48 h. PCB contamination is a present-day threat to the health of individual organisms and ecosystems in the polar region. We showed that 11 of 14 genes responded to PCB treatment at transcriptional levels, with the most dramatic upregulation observed in the hsp70.5 gene. In this paper, we summarize the expressed cDNA information and discuss its potential use in ecotoxicological genomic studies on PCB exposure.

Keywords

Arctic sea urchin Strongylocentrotus droebachiensis Expressed sequence tag Polychlorinated biphenyls Aroclor 1254 

Notes

Acknowledgments

We thank Dr. Hans-U. Dahms for his comments on the manuscript and also thank three anonymous reviewers for their valuable comments. This work was supported by a grant from KOPRI (PE08040) and also supported by a grant of K-POD (2014) funded to Jae-Seong Lee.

Supplementary material

300_2014_1507_MOESM1_ESM.xlsx (7.2 mb)
Supplementary material 1 (XLSX 7365 kb)

References

  1. Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A 138:405–415CrossRefGoogle Scholar
  2. Adams MD, Kelley JM, Gocayne JD, Dubnick M, Polymeropoulos MH, Xiao H, Merril CR, Wu A, Olde B, Moreno RF et al (1991) Complementary DNA sequencing: expressed sequence tags and human genome project. Science 252:1651–1656PubMedCrossRefGoogle Scholar
  3. Arctic Monitoring and Assessment Programme (2004) AMAP assessment 2002: Persistent organic pollutants in the Arctic. AMAP, Oslo, NorwayGoogle Scholar
  4. Bard SM (1999) Global transport of anthropogenic contaminants and the consequences for the Arctic marine ecosystem. Mar Pollut Bull 38:356–379CrossRefGoogle Scholar
  5. Beuchel F, Gulliksen B (2008) Temporal patterns of benthic community development in an Arctic fjord (Kongsfjorden, Svalbard): results of a 24-year manipulation study. Polar Biol 31:913–924CrossRefGoogle Scholar
  6. Blanchette B, Feng X, Singh BR (2007) Marine glutathione S-transferases. Mar Biotechnol 9:513–542PubMedCrossRefGoogle Scholar
  7. Blom S, Förlin L (1998) Effects of PCB on xenobiotic biotransformation enzyme activities in the liver and 21-hydroxylation in the head kidney of juvenile rainbow trout. Aquat Toxicol 39:215–230CrossRefGoogle Scholar
  8. Bosnjak I, Uhlinger KR, Heim W, Smital T, Franekić-Colić J, Coale K, Epel D, Hamdoun A (2009) Multidrug efflux transporters limit accumulation of inorganic, but not organic, mercury in sea urchin embryos. Environ Sci Technol 43:8374–8380PubMedCentralPubMedCrossRefGoogle Scholar
  9. De Zoysa M, Ekanayake PM, Kang H-S, Lee J, Jee Y, Lee Y-H, Kim S-J (2009) Disk abalone, Haliotis discus discus, CuZn-superoxide dismutase cDNA and its transcriptional induction by Aroclor 1254. J World Aquacult Soc 40:643–658CrossRefGoogle Scholar
  10. Dehn L-A, Follmann EH, Thomas DL, Sheffield GG, Rosa C, Duffy LK, O’Hara TM (2006) Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci Total Environ 362:103–123PubMedCrossRefGoogle Scholar
  11. Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679PubMedCentralPubMedCrossRefGoogle Scholar
  12. Durou C, Poirier L, Amiard JC, Budzinski H, Gnassia-Barelli M, Lemenach K, Peluhet L, Mouneyrac C, Roméo M, Amiard-Triquet C (2007) Biomonitoring in a clean and a multi-contaminated estuary based on biomarkers and chemical analyses in the endobenthic worm Nereis diversicolor. Environ Pollut 148:445–458PubMedCrossRefGoogle Scholar
  13. Fant ML, Nyman M, Helle E, Rudbäck E (2001) Mercury, cadmium, lead and selenium in ringed seals (Phoca hispida) from the Baltic Sea and from Svalbard. Environ Pollut 111:493–501PubMedCrossRefGoogle Scholar
  14. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  15. Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449PubMedGoogle Scholar
  16. Fogg GE (1998) The biology of polar habitats. Oxford University Press, New YorkGoogle Scholar
  17. Gabrielsen GW, Skaare JU, Polder A, Bakken V (1995) Chlorinated hydrocarbons in Glaucous Gulls (Larus hyperboreus) at the southern part of Svalbard. Sci Tot Environ 160(161):337–346CrossRefGoogle Scholar
  18. Giesy JP, Kannan K (1998) Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): implications for risk assessment. Crit Rev Toxicol 28:511–569PubMedCrossRefGoogle Scholar
  19. Goerke H, Weber K, Bornemann H, Ramdohr S, Plotz J (2004) Increasing levels and biomagnification of persistent organic pollutants (POPs) in Antarctic biota. Mar Pollut Bull 48:295–302PubMedCrossRefGoogle Scholar
  20. Goldstone JV, Hamdoun A, Cole BJ, Howard-Ashby M, Nebert DW, Scally M, Dean M, Epel D, Hahn ME, Stegeman JJ (2006) The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Dev Biol 300:366–384PubMedCentralPubMedCrossRefGoogle Scholar
  21. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750PubMedCentralPubMedCrossRefGoogle Scholar
  22. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88PubMedCrossRefGoogle Scholar
  23. Hennig B, Hammock BD, Slim R, Toborek M, Saraswathi V, Robertson LW (2002) PCB-induced oxidative stress in endothelial cells: modulation by nutrients. Int J Hyg Environ Health 205:95–102PubMedCrossRefGoogle Scholar
  24. Hop H, Pearson T, Hegseth EN, Kovacs KM, Weslawski JM, Wiencke C, Kwasniewski S, Eiane K, Leakey R, Cochrane S, Zajaczkowski M, Lonne OJ, Mehlum F, Lydersen C, Gulliksen B, Falk-Petersen S, Poltermann M, Wangberg S-A, Kendall M, Bischof KY, Voronkov A, Kovaltchouk NA, Gabrielsen GW, Wlodarska-Kowalczuk M, Wiktor J, di Prisco G, Estoppey A, Papucci C, Gerland S (2002) The marine ecosystem of Kongsfjorden, Svalbard. Polar Res 21:167–208CrossRefGoogle Scholar
  25. Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predicts population decline. Ecotoxicol Environ Saf 54:366–374PubMedCrossRefGoogle Scholar
  26. Kim R-O, Kim B-M, Jeong C-B, Nelson DR, Lee J-S, Rhee J-S (2013) Expression pattern of entire cytochrome P450 genes and response of defensomes in the benzo[a]pyrene-exposed monogonont rotifer Brachionus koreanus. Environ Sci Technol 47:13804–13812PubMedCrossRefGoogle Scholar
  27. Kreiling JA, Creton R, Reinisch C (2007) Early embryonic exposure to polychlorinated biphenyls disrupts heat-shock protein 70 cognate expression in zebrafish. J Toxicol Environ Health A 70:1005–1013PubMedCrossRefGoogle Scholar
  28. Kumar KS, Kannan K, Corsolini S, Evans T, Giesy JP, Nakanishi J, Masunaga S (2002) Polychlorinated dibenzo-p-dioxins, dibenzofurans and polychlorinated biphenyls in polar bear, penguin and south polar skua. Environ Pollut 119:151–161PubMedCrossRefGoogle Scholar
  29. Lee YH, Huang GM, Cameron RA, Graham G, Davidson EH, Hood L, Britten RJ (1999) EST analysis of gene expression in early cleavage-stage sea urchin embryos. Development 126:3857–3867PubMedGoogle Scholar
  30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  31. Machala M, Drabek P, Neca J, Kolarova J, Svobodova Z (1998) Biochemical markers for differentiation of exposures to nonplanar polychlorinated biphenyls, organochlorine pesticides, or 2,3,7, 8-tetrachlorodibenzo-p-dioxin in trout liver. Ecotoxicol Environ Saf 41:107–111PubMedCrossRefGoogle Scholar
  32. Margulies M et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedCentralPubMedGoogle Scholar
  33. Martín-Díaz ML, Blasco J, Sales D, Delvalls TA (2007) Biomarkers study for sediment quality assessment in Spanish ports using the crab Carcinus maenas and the clam Ruditapes philippinarum. Arch Environ Contam Toxicol 53:66–76PubMedCrossRefGoogle Scholar
  34. Morehouse LA, Bumpus JA, Voorman R, Thomas CE, Aust SD (1984) Superoxide production by reconstituted cytochrome P450-dependent mixed function oxidases. FASEB J 43:355Google Scholar
  35. Moreira SM, Guilhermino L (2005) The use of Mytilus galloprovincialis acetylcholinesterase and glutathione S-transferases activities as biomarkers of environmental contamination along the northwest Portuguese coast. Environ Monit Assess 105:309–325PubMedCrossRefGoogle Scholar
  36. Muir DCG, Norstrom RJ, Simon M (1988) Organochlorine contaminants in Arctic marine food chains: Accumulation of specific polychlorinated biphenyls and chlordane- related compounds. Environ Sci Technol 14:1071–1079CrossRefGoogle Scholar
  37. Muir DCG, Braune B, DeMarch B, Norstrom R, Wagemann R, Lockhart L, Hargrave B, Bright D, Addison R, Payne J, Reimer K (1999) Spatial and temporal trends and effects of contaminants in the Canadian Arctic marine ecosystem: a review. Sci Total Environ 230:83–144PubMedCrossRefGoogle Scholar
  38. Nahrgang J, Camus L, Gonzalez P, Goksøyr A, Christiansen JS, Hop H (2009) PAH biomarker responses in polar cod (Boreogadus saida) exposed to benzo(a)pyrene. Aquat Toxicol 94:309–319PubMedCrossRefGoogle Scholar
  39. Noël M, Loseto LL, Helbing CC, Veldhoen N, Dangerfield NJ, Ross PS (2014) PCBs are associated with altered gene transcript profiles in Arctic beluga whales (Delphinapterus leucas). Environ Sci Technol 48:2942–2951PubMedCrossRefGoogle Scholar
  40. Oakley GG, Devanaboyina U, Robertson LW, Gupta RC (1996) Oxidative DNA damage induced by activation of polychlorinated biphenyls (PCBs): implications for PCB-induced oxidative stress in breast cancer. Chem Res Toxicol 9:1285–1292PubMedCrossRefGoogle Scholar
  41. Oehme M (1991) Further evidence for long-range transport of polychlorinated aromates and pesticides: North America and Eurasia to the Arctic. Ambio 20:293–297Google Scholar
  42. Otto DM, Moon TW (1995) 3,3′,4,4′-tetrachlorobiphenyl effects on antioxidant enzymes and glutathione status in different tissues of rainbow trout. Pharmacol Toxicol 77:281–287PubMedCrossRefGoogle Scholar
  43. Otto DM, Moon TW (1996) Phase I and II enzymes and antioxidant responses in different tissues of brown bullheads from relatively polluted and non-polluted systems. Arch Environ Contam Toxicol 31:141–147PubMedCrossRefGoogle Scholar
  44. Park H, Ahn I-Y, Kim H, Lee J, Shin SC (2009a) Glutathione S-transferase as a biomarker in the Antarctic bivalve Laternula elliptica after exposure to the polychlorinated biphenyl mixture Aroclor 1254. Comp Biochem Physiol C 150:528–536Google Scholar
  45. Park H, Ahn I-Y, Lee JK, Shin SC, Lee J, Choy E-J (2009b) Molecular cloning, characterization, and the response of manganese superoxide dismutase from the Antarctic bivalve Laternula elliptica to PCB exposure. Fish Shellfish Immunol 27:522–528PubMedCrossRefGoogle Scholar
  46. Pastore A, Federici G, Bertini E, Piemonte F (2003) Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta 333:19–39PubMedCrossRefGoogle Scholar
  47. Pérez-López M, Nóvoa-Valiñas MC, Melgar-Riol MJ (2002a) Induction of cytosolic glutathione S-transferases from Atlantic eel (Anguilla anguilla) after intraperitoneal treatment with polychlorinated biphenyls. Sci Total Environ 297:141–151PubMedCrossRefGoogle Scholar
  48. Pérez-López M, Nóvoa-Valiñas MC, Melgar-Riol MJ (2002b) Glutathione S-transferase cytosolic isoforms as biomarkers of polychlorinated biphenyl (Arochlor-1254) experimental contamination in rainbow trout. Toxicol Lett 136:97–106PubMedCrossRefGoogle Scholar
  49. Poustka AJ, Groth D, Hennig S, Thamm S, Cameron A, Beck A, Reinhardt R, Herwig R, Panopoulou G, Lehrach H (2003) Generation, annotation, evolutionary analysis, and database integration of 20,000 unique sea urchin EST clusters. Genome Res 13:2736–2746PubMedCentralPubMedCrossRefGoogle Scholar
  50. Poustka AJ, Kühn A, Groth D, Weise V, Yaguchi S, Burke RD, Herwig R, Lehrach H, Panopoulou G (2007) A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. Genome Biol 8:R85PubMedCentralPubMedCrossRefGoogle Scholar
  51. Rhee J-S, Lee Y-M, Hwang D-S, Won E-J, Raisuddin S, Shin KH, Lee J-S (2007) Molecular cloning, expression, biochemical characteristics, and biomarker potential of theta class glutathione S-transferase (GST-T) from the polychaete Neanthes succinea. Aquat Toxicol 83:104–115PubMedCrossRefGoogle Scholar
  52. Rhee J-S, Kim B-M, Kim R-O, Choi B-S, Choi I-Y, Lee Y-M, Lee J-S (2011) Analysis of expressed sequence tags from the liver and ovary of the euryhaline hermaphroditic fish, Kryptolebias marmoratus. Comp Biochem Physiol D 6:244–255Google Scholar
  53. Rhee J-S, Kim B-M, Jeong C-B, Horiguchi T, Lee Y-M, Kim I-C, Lee J-S (2012a) Immune gene mining by pyrosequencing in the rockshell, Thais clavigera. Fish Shellfish Immunol 32:700–710PubMedCrossRefGoogle Scholar
  54. Rhee J-S, Ki J-S, Hwang D-S, Park H, Ahn I-Y, Lee J-S (2012b) Complete mitochondrial genome of the Arctic green sea urchin Strongylocentrotus droebachiensis (Strongylocentrotidae, Echinoidea). Mitochondrial DNA 23:369–370PubMedCrossRefGoogle Scholar
  55. Samanta MP, Tongprasit W, Istrail S, Cameron RA, Tu Q, Davidson EH, Stolc V (2006) The transcriptome of the sea urchin embryo. Science 314:960–962PubMedCrossRefGoogle Scholar
  56. Schlezinger JJ, Stegeman JJ (2001) Induction and suppression of cytochrome P4501A by 3,3′,4,4′,5-pentachlorobiphenyl and its relationship to oxidative stress in the marine fish scup (Stenotomus chrysops). Aquat Toxicol 52:101–115PubMedCrossRefGoogle Scholar
  57. Schlezinger JJ, Struntz WD, Goldstone JV, Stegeman JJ (2006) Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquat Toxicol 77:422–432PubMedCrossRefGoogle Scholar
  58. Sea Urchin Genome Sequencing Consortium (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952PubMedCentralCrossRefGoogle Scholar
  59. Shipp LE, Hamdoun A (2012) ATP-binding cassette (ABC) transporter expression and localization in sea urchin development. Dev Dyn 241:1111–1124PubMedCentralPubMedCrossRefGoogle Scholar
  60. Sies H (1999) Glutathione and its role in cellular functions. Free Rad. Biol. Med. 27:916–921PubMedCrossRefGoogle Scholar
  61. Skaare JU, Markussen NH, Norheim G, Hauge S, Holt G (1990) Levels of polychlorinated biphenyls, organochlorine pesticides, mercury, cadmium, copper, selenium, arsenic, and zinc in the harbour seal, Phoca vitulina, in Norwegians waters. Environ Pollut 66:309–324PubMedCrossRefGoogle Scholar
  62. Slim R, Toborek M, Robertson LW, Lehmler HJ, Hennig B (2000) Cellular glutathione status modulates polychlorinated biphenyl-induced stress response and apoptosis in vascular endothelial cells. Toxicol Appl Pharmacol 166:36–42PubMedCrossRefGoogle Scholar
  63. Tu Q, Cameron RA, Worley KC, Gibbs RA, Davidson EH (2012) Gene structure in the sea urchin Strongylocentrotus purpuratus based on transcriptome analysis. Genome Res 22:2079–2087PubMedCentralPubMedCrossRefGoogle Scholar
  64. Tu Q, Cameron RA, Davidson EH (2014) Quantitative developmental transcriptomes of the sea urchin Strongylocentrotus purpuratus. Dev Biol 385:160–167PubMedCrossRefGoogle Scholar
  65. Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237:408–414PubMedCrossRefGoogle Scholar
  66. Van den Berg M, Birnbaum L, Bosveld AT, Brunström B, Cook P, Feeley M, Giesy JP, Hanberg A, Hasegawa R, Kennedy SW, Kubiak T, Larsen JC, van Leeuwen FX, Liem AK, Nolt C, Peterson RE, Poellinger L, Safe S, Schrenk D, Tillitt D, Tysklind M, Younes M, Waern F, Zacharewski T (1998) Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect 106:775–792PubMedCentralPubMedCrossRefGoogle Scholar
  67. van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149PubMedCrossRefGoogle Scholar
  68. Vega RL, Epel D (2004) Stress-induced apoptosis in sea urchin embryogenesis. Mar Environ Res 58:799–802PubMedCrossRefGoogle Scholar
  69. Verde C, Parisi E, di Prisco G (2006) The evolution of thermal adaptation in polar fish. Gene 385:137–145PubMedCrossRefGoogle Scholar
  70. Wagemann R, Innes S, Richard PR (1996) Overview and regional and temporal differences of heavy metals in Arctic whales and ringed seals in the Canadian Arctic. Sci Tot Environ 186:41–66CrossRefGoogle Scholar
  71. Wania F, Mackay D (1993) Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions. Ambio 22:10–18Google Scholar
  72. Wei Z, Angerer RC, Angerer LM (2006) A database of mRNA expression patterns for the sea urchin embryo. Dev Biol 300:476–484PubMedCentralPubMedCrossRefGoogle Scholar
  73. Wiens M, Koziol C, Hassanein HMA, Batel R, Schröder HC, Müller WE (1998) Induction of gene expression of the chaperones 14-3-3 and HSP70 by PCB 118 (2,3′, 4,4′, 5-pentachlorobiphenyl) in the marine sponge Geodia cydonium: novel biomarkers for polychlorinated biphenyls. Mar Ecol Prog Ser 165:247–257CrossRefGoogle Scholar
  74. Wiens M, Ammar MS, Nawar AH, Koziol C, Hassanein HM, Eisinger M, Müller IM, Müller WE (2000) Induction of heat-shock (stress) protein gene expression by selected natural and anthropogenic disturbances in the octocoral Dendronephthya klunzingeri. J Exp Mar Biol Ecol 245:265–276PubMedCrossRefGoogle Scholar
  75. Yadetie F, Butcher S, Førde HE, Campsteijn C, Bouquet JM, Karlsen OA, Denoeud F, Metpally R, Thompson EM, Manak JR, Goksøyr A, Chourrout D (2012) Conservation and divergence of chemical defense system in the tunicate Oikopleura dioica revealed by genome wide response to two xenobiotics. BMC Gen 2:55CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Jae-Sung Rhee
    • 1
  • Bo-Mi Kim
    • 2
  • Beom-Soon Choi
    • 3
  • Ik-Young Choi
    • 3
  • Hyun Park
    • 4
  • In-Young Ahn
    • 5
  • Jae-Seong Lee
    • 2
  1. 1.Department of Marine Science, College of Natural SciencesIncheon National UniversityIncheonSouth Korea
  2. 2.Department of Biological Sciences, College of ScienceSungkyunkwan UniversitySuwonSouth Korea
  3. 3.National Instrumentation Center for Environmental Management, College of Agriculture and Life SciencesSeoul National UniversitySeoulSouth Korea
  4. 4.Division of Polar Life SciencesKorea Polar Research InstituteIncheonSouth Korea
  5. 5.Division of Polar Ocean EnvironmentKorea Polar Research InstituteIncheonSouth Korea

Personalised recommendations