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.
Similar content being viewed by others
References
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 138:405–415
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 252:1651–1656
Arctic Monitoring and Assessment Programme (2004) AMAP assessment 2002: Persistent organic pollutants in the Arctic. AMAP, Oslo, Norway
Bard SM (1999) Global transport of anthropogenic contaminants and the consequences for the Arctic marine ecosystem. Mar Pollut Bull 38:356–379
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 31:913–924
Blanchette B, Feng X, Singh BR (2007) Marine glutathione S-transferases. Mar Biotechnol 9:513–542
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 39:215–230
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 43:8374–8380
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 40:643–658
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 362:103–123
Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679
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 148:445–458
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 111:493–501
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449
Fogg GE (1998) The biology of polar habitats. Oxford University Press, New York
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):337–346
Giesy JP, Kannan K (1998) Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): implications for risk assessment. Crit Rev Toxicol 28:511–569
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 48:295–302
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 300:366–384
Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750
Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88
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 205:95–102
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 21:167–208
Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predicts population decline. Ecotoxicol Environ Saf 54:366–374
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 47:13804–13812
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 70:1005–1013
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 119:151–161
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 126:3857–3867
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
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 41:107–111
Margulies M et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380
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 53:66–76
Morehouse LA, Bumpus JA, Voorman R, Thomas CE, Aust SD (1984) Superoxide production by reconstituted cytochrome P450-dependent mixed function oxidases. FASEB J 43:355
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 105:309–325
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 14:1071–1079
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 230:83–144
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 94:309–319
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 48:2942–2951
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 9:1285–1292
Oehme M (1991) Further evidence for long-range transport of polychlorinated aromates and pesticides: North America and Eurasia to the Arctic. Ambio 20:293–297
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 77:281–287
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 31:141–147
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 150:528–536
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 27:522–528
Pastore A, Federici G, Bertini E, Piemonte F (2003) Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta 333:19–39
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 297:141–151
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 136:97–106
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 13:2736–2746
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:R85
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 83:104–115
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 6:244–255
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 32:700–710
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 23:369–370
Samanta MP, Tongprasit W, Istrail S, Cameron RA, Tu Q, Davidson EH, Stolc V (2006) The transcriptome of the sea urchin embryo. Science 314:960–962
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 52:101–115
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 77:422–432
Sea Urchin Genome Sequencing Consortium (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952
Shipp LE, Hamdoun A (2012) ATP-binding cassette (ABC) transporter expression and localization in sea urchin development. Dev Dyn 241:1111–1124
Sies H (1999) Glutathione and its role in cellular functions. Free Rad. Biol. Med. 27:916–921
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 66:309–324
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 166:36–42
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 22:2079–2087
Tu Q, Cameron RA, Davidson EH (2014) Quantitative developmental transcriptomes of the sea urchin Strongylocentrotus purpuratus. Dev Biol 385:160–167
Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237:408–414
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 106:775–792
van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149
Vega RL, Epel D (2004) Stress-induced apoptosis in sea urchin embryogenesis. Mar Environ Res 58:799–802
Verde C, Parisi E, di Prisco G (2006) The evolution of thermal adaptation in polar fish. Gene 385:137–145
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 186:41–66
Wania F, Mackay D (1993) Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions. Ambio 22:10–18
Wei Z, Angerer RC, Angerer LM (2006) A database of mRNA expression patterns for the sea urchin embryo. Dev Biol 300:476–484
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 165:247–257
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 245:265–276
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 2:55
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rhee, JS., Kim, BM., Choi, BS. et al. Transcriptome information of the Arctic green sea urchin and its use in environmental monitoring. Polar Biol 37, 1133–1144 (2014). https://doi.org/10.1007/s00300-014-1507-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-014-1507-9