Skip to main content

Advertisement

SpringerLink
Log in

Expressed sequence tag library of the marine green alga Tetraselmis suecica: a focus on stress-related genes for marine pollution

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The marine green microalga, Tetraselmis suecica, is an important food source for aquaculture, lipid source for biofuel production, and a potential model organism for toxicity assays because of its rapid growth and ability to produce useful chemicals. In order to gain molecular toxicogenomic insights, we determined expressed sequence tags (ESTs) of T. suecica by pyrosequencing, and attained 741 K reads, including 290 Mb of cDNA information. Upon data processing, 24,651 contigs and 19,072 non-overlapping fragments were acquired and deposited to the NCBI non-redundant and gene ontology databases. Of these, 11,292 contigs and 1848 singletons were annotated. From the EST data, we found that many previously identified stress-responsive protein-coding genes were included. The data were further investigated with a focus on heat shock protein (HSP) gene families, with most characterized HSP genes present in our ESTs. In addition, the expression of HSP70 and HSP90 was significantly increased after T. suecica cells were exposed to metal contaminants. This work expands our understanding of stress-related genomics of T. suecica and further evaluates a potential use of oxidative stress-related genes as biomarkers, in particular HSP involvement in environmental genomics and marine toxicological assessment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abu Laban N, Tan B, Dao A, Foght J (2015) Draft genome sequence of uncultivated toluene-degrading Desulfobulbaceae bacterium Tol-SR, obtained by stable isotope probing using [13C6]toluene. Genome Announc 3:e01423–e01414

    PubMed  PubMed Central  Google Scholar 

  • Alsterberg C, Eklöf JS, Gamfeldt L, Havenhand JN, Sundbäck K (2013) Consumers mediate the effects of experimental ocean acidification and warming on primary producers. Proc Natl Acad Sci U S A 110:8603–8608

    Article  PubMed  PubMed Central  Google Scholar 

  • Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U, Brodie EL, Williams KH, Hubbard SS, Banfield JF (2016) Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun 7:13219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  PubMed  CAS  Google Scholar 

  • Asamizu E, Nakamura Y, Sato S, Fukuzawa H, Tabata S (1999) A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Res 6:369–373

    Article  PubMed  Google Scholar 

  • Asamizu E, Miura K, Kucho K, Inoue Y, Fukuzawa H, Ohyama K, Nakamura Y, Tabata S (2000) Generation of expressed sequence tags from low-CO2 and high-CO2 adapted cells of Chlamydomonas reinhardtii. DNA Res 7:305–307

    Article  PubMed  Google Scholar 

  • Austin B, Baudet E, Stobie M (1992) Inhibition of bacterial fish pathogens by Tetraselmis suecica. J Fish Dis 15:55–61

    Article  Google Scholar 

  • Becker B, Becker D, Kamerling JP, Melkonian M (1991) 2-keto sugar acids in green flagellates: a chemical marker for prasinophycean scales. J Phycol 27:498–504

    Article  CAS  Google Scholar 

  • Becker B, Feja N, Melkonian M (2001) Analysis of expressed sequence tags (ESTs) from the scaly green flagellate Scherffelia dubia Pascher emend. Melkonian et Preisig. Protist 152:139–147

    Article  PubMed  CAS  Google Scholar 

  • Bergeron H, Labbé D, Turmel C, Lau PC (1998) Cloning, sequence and expression of a linear plasmid-based and a chromosomal homolog of chloroacetaldehyde dehydrogenase-encoding genes in Xanthobacter autotrophicus GJ10. Gene 207:9–18

    Article  PubMed  CAS  Google Scholar 

  • Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD, Gurnon J, Ladunga I, Lindquist E, Lucas S, Pangilinan J, Pröschold T, Salamov A, Schmutz J, Weeks D, Yamada T, Lomsadze A, Borodovsky M, Claverie JM, Grigoriev IV, van Etten JL (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13:R39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blanc-Mathieu R, Verhelst B, Derelle E, Rombauts S, Bouget FY, Carré I, Château A, Eyre-Walker A, Grimsley N, Moreau H, Piégu B, Rivals E, Schackwitz W, van de Peer Y, Piganeau G (2014) An improved genome of the model marine alga Ostreococcus tauri unfolds by assessing Illumina de novo assemblies. BMC Genomics 15:1103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bowler C, Allen AE, Badger JH et al. (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

  • Bucciarelli T, Sacchetta P, Amicarelli F, Petruzzelli R, Melino S, Rotilio D, Celli N, Di Ilio C (2002) Amino acid sequence of the major form of toad liver glutathione transferase. Int J Biochem Cell Biol 34:1286–1290

    Article  PubMed  CAS  Google Scholar 

  • Carballo-Cardenas EC, Tuan PM, Janssen M, Wijffels RH (2003) Vitamin E (alpha-tocopherol) production by the marine microalgae Dunaliella tertiolecta and Tetraselmis suecica in batch cultivation. Biomol Eng 20:139–147

    Article  PubMed  CAS  Google Scholar 

  • Cerný M, Jedelský PL, Novák J, Schlosser A, Brzobohatý B (2014) Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant Cell Environ 37:1641–1655

    Article  PubMed  CAS  Google Scholar 

  • Cirulis JT, Scott JA, Ross GM (2013) Management of oxidative stress by microalgae. Can J Physiol Pharmacol 91:15–21

    Article  PubMed  CAS  Google Scholar 

  • Cock JM, Sterck L, Rouzé P et al. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621

  • Cordero BF, Obraztsova I, Martin L, Couso I, Leon R, Vargas MA, Rodriguez HM (2010) Isolation and characterization of a lycopene β-cyclase gene from the astaxanthin-producing green alga Chlorella zofingiensis (Chlorophyta). J Phycol 46:1229–1238

    Article  CAS  Google Scholar 

  • Cordero BF, Couso I, León R, Rodríguez H, Vargas MA (2011) Enhancement of carotenoids biosynthesis in Chlamydomonas reinhardtii by nuclear transformation using a phytoene synthase gene isolated from Chlorella zofingiensis. Appl Microbiol Biotechnol 91:341–351

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cui Y, Qin S, Jiang P (2014) Chloroplast transformation of Platymonas (Tetraselmis) subcordiformis with the bar gene as selectable marker. PLoS One 9:e98607

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Maio A (1999) Heat shock proteins. Facts, thoughts, and dreams. Shock 11:1–12

    Article  PubMed  Google Scholar 

  • Ebenezer V, Ki JS (2013) Quantification of the sub-lethal toxicity of metals and endocrine-disrupting chemicals to the marine green microalga Tetraselmis suecica. Fish Aquatic Sci 16:187–194

    Article  CAS  Google Scholar 

  • Ebenezer V, Ki JS (2014) Quantification of toxic effects of the organochlorine insecticide endosulfan on marine green algae, diatom and dinoflagellate. Indian J Geo-marine Sci 43:393–399

    Google Scholar 

  • Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB (2009) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas fir (Pseudotsuga menziesii var. menziesii). Genetics 183:289–298

    Article  PubMed  PubMed Central  Google Scholar 

  • Eguchi K, Nagase H, Ozawa M, Endoh YS, Goto K, Hirata K, Miyamoto K, Yoshimura H (2004) Evaluation of antimicrobial agents for veterinary use in the ecotoxicity test using microalgae. Chemosphere 57:1733–1738

    Article  PubMed  CAS  Google Scholar 

  • Fabregas J, Abalde J, Herrero C, Cabezas B, Veiga M (1984) Growth of the marine microalga Tetraselmis suecica in batch cultures with different salinities and nutrient concentrations. Aquaculture 42:207–215

    Article  Google Scholar 

  • Featherston J, Arakaki Y, Hanschen ER, Ferris PJ, Michod RE, Olson BJSC, Nozaki H, Durand PM (2017) The 4-celled Tetrabaena socialis nuclear genome reveals the essential components for genetic control of cell number at the origin of multicellularity in the volvocine lineage. Mol Biol Evol. https://doi.org/10.1093/molbev/msx332

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719

    Article  PubMed  CAS  Google Scholar 

  • Fon-Sing S, Borowitzka MA (2016) Isolation and screening of euryhaline Tetraselmis spp. suitable for large-scale outdoor culture in hypersaline media for biofuels. J Appl Phycol 28:1–14

    Article  CAS  Google Scholar 

  • Franklin NM, Stauber JL, Apte SC, Lim RP (2002) Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays. Environ Toxicol Chem 21:742–751

    Article  PubMed  CAS  Google Scholar 

  • Fu M, Zou Z, Liu S, Lin P, Wang Y, Zhang Z (2012) Selenium-dependent glutathione peroxidase gene expression during gonad development and its response to LPS and H2O2 challenge in Scylla paramamosain. Fish Shellfish Immunol 33:532–542

  • Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y, Duan Z, Hu X, Xie XQ, Zhou G, Peng G, Luo Z, Huang W, Wang B, Fang W, Wang S, Zhong Y, Ma LJ, St. Leger RJ, Zhao GP, Pei Y, Feng MG, Xia Y, Wang C (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7:e1001264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garbayo I, Cuaresma M, Vilchez C, Vega JM (2008) Effect of abiotic stress on the production of lutein and beta-carotene by Chlamydomonas acidophila. Process Biochem 43:1158–1161

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Grossman AR, Harris EE, Hauser C, Lefebvre PA, Martinez D, Rokhsar D, Shrager J, Silflow CD, Stern D, Vallon O, Zhang Z (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot Cell 2:1137–1150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Guiry MD, Guiry GM (2017) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed 10 March 2017

  • Guo R, Ki JS (2012a) Differential transcription of heat shock protein 90 (HSP 90) in the dinoflagellate Prorocentrum minimum by copper and endocrine-disrupting chemicals. Ecotoxicology 21:1448–1457

    Article  PubMed  CAS  Google Scholar 

  • Guo R, Ki JS (2012b) Evaluation and validation of internal control genes for studying gene expression in the dinoflagellate Prorocentrum minimum using real-time PCR. Eur J Protistol 48:199–206

    Article  PubMed  Google Scholar 

  • Guo R, Ki JS (2013) Characterization of a novel catalase–peroxidase (KATG) gene from the dinoflagellate Prorocentrum minimum. J Phycol 49:1011–1016

    PubMed  CAS  Google Scholar 

  • Guo R, Lee MA, Ki JS (2013) Different transcriptional responses of heat shock protein 70/90 in the marine diatom Ditylum brightwellii exposed to metal compounds and endocrine-disrupting chemicals. Chemosphere 92:535–543

    Article  PubMed  CAS  Google Scholar 

  • Guo R, Ebenezer V, Ki JS (2014) PmMGST3, a novel microsomal glutathione S-transferase gene in the dinoflagellate Prorocentrum minimum, is a potential biomarker of oxidative stress. Gene 546:378–385

    Article  PubMed  CAS  Google Scholar 

  • Guo R, Youn SH, Ki JS (2015) Heat shock protein 70 and 90 genes in the harmful dinoflagellate Cochlodinium polykrikoides: genomic structures and transcriptional responses to environmental stresses. Int J Genom Article ID 484626:1–12

    Google Scholar 

  • Guo R, Lim WA, Ki JS (2016a) Genome-wide analysis of transcription and photosynthesis inhibition in the harmful dinoflagellate Prorocentrum minimum in response to the biocide copper sulfate. Harmful Algae 57:27–38

    Article  CAS  PubMed  Google Scholar 

  • Guo R, Wang H, Suh YS, Ki JS (2016b) Transcriptomic profiles reveal the genome-wide responses of the harmful dinoflagellate Cochlodinium polykrikoides when exposed to the algicide copper sulfate. BMC Genomics 17:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo R, Ebenezer V, Wang H, Ki JS (2017) Chlorine affects photosystem II and modulates the transcriptional levels of photosynthesis-related genes in the dinoflagellate Prorocentrum minimum. J Appl Phycol 29:153–163

    Article  CAS  Google Scholar 

  • Harker M, Hirschberg J (1997) Biosynthesis of ketocarotenoids in transgenic cyanobacteria expressing the algal gene for β-C-4-oxygenase, crtO. FEBS Lett 404:129–134

    Article  PubMed  CAS  Google Scholar 

  • Hu P, Tom L, Singh A, Thomas BC, Baker BJ, Piceno YM, Andersen GL, Banfield JF (2016) Genome-resolved metagenomic analysis reveals roles for candidate phyla and other microbial community members in biogeochemical transformations in oil reservoirs. mBio 7:1 e01669–15

  • Hunter SS, Yano H, Loftie-Eaton W, Hughes J, De Gelder L, Stragier P, De Vos P, Settles ML, Top EM (2014) Draft genome sequence of Pseudomonas moraviensis R28-S. Genome Announc 2:e00035–e00014

    Article  PubMed  PubMed Central  Google Scholar 

  • Irianto A, Austin B (2002) Probiotics in aquaculture. J Fish Dis 25:633–642

    Article  Google Scholar 

  • Ishikawa T, Tajima N, Nishikawa H, Gao Y, Rapolu M, Shibata H, Sawa Y, Shigeoka S (2010) Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. Biochem J 426:125–134

    Article  PubMed  CAS  Google Scholar 

  • Istvánek J, Jaros M, Krenek A, Řepková J (2014) Genome assembly and annotation for red clover (Trifolium pratense; Fabaceae). Am J Bot 101:327–337

    Article  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin CS, Guill K, Regulski M, Kumari S, Olson A, Gent J, Schneider KL, Wolfgruber TK, May MR, Springer NM, Antoniou E, McCombie W, Presting GG, McMullen M, Ross-Ibarra J, Dawe RK, Hastie A, Rank DR, Ware D (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527

    PubMed  CAS  Google Scholar 

  • Jinkerson RE, D’Adamos S, Posewitz MC. The transcriptome of the halophilic microalga Tetraselmis sp. GSL018 isolated from the great salt lake, Utah https://www.ncbi.nlm.nih.gov/nuccore/?term=Tetraselmis%20sp.%20GSL018. Accessed 10 March 2017

  • Jones AC, Monroe EA, Podell S, Hess WR, Klages S, Esquenazi E, Niessen S, Hoover H, Rothmann M, Lasken RS, Yates JR, Reinhardt R, Kube M, Burkart MD, Allen EE, Dorrestein PC, Gerwick WH, Gerwick L (2011) Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula. Proc Natl Acad Sci U S A 108:8815–8820

    Article  PubMed  PubMed Central  Google Scholar 

  • Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperon 14:105–111

    Article  CAS  Google Scholar 

  • Kim IS, Kim HY, Shin SY, Kim YS, Lee DH, Park KM, Yoon HS (2010) A cyclophilin a CPR1 overexpression enhances stress acquisition in Saccharomyces cerevisiae. Mol Cells 29:567–574

    Article  PubMed  CAS  Google Scholar 

  • Kolinko S, Richter M, Glöckner FO, Brachmann A, Schüler D (2016) Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes. Environ Microbiol 18:21–37

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  Google Scholar 

  • Li T, Shi C, Gan Z, Shi X (2009) Cloning and analysis of the gene encoding lycopene epsilon cyclase in Chlorella protothecoides CS-41. Wei Sheng Wu Xue Bao 49:1180–1189

    PubMed  CAS  Google Scholar 

  • Lin DT, Lechleiter JD (2002) Mitochondrial targeted cyclophilin D protects cells from cell death by peptidyl prolyl isomerization. J Biol Chem 277:31134–31141

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Ma X, Yu H, Fang D, Li Y, Wang X, Wang W, Dong Y, Xiao B (2016) Genomes and virulence difference between two physiological races of Phytophthora nicotianae. Gigascience 5:3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lluisma AO, Ragan MA (1997) Expressed sequence tags (ESTs) from the marine red alga Gracilaria gracilis. J Appl Phycol 9:287–293

    Article  CAS  Google Scholar 

  • Mainali HR, Chapman P, Dhaubhadel S (2014) Genome-wide analysis of Cyclophilin gene family in soybean (Glycine max). BMC Plant Biol 14:282

    Article  PubMed  PubMed Central  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

  • Miller IJ, Weyna TR, Fong SS, Lim-Fong GE, Kwan JC (2016) Single sample resolution of rare microbial dark matter in a marine invertebrate metagenome. Sci Rep 6:34362

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miyasaka H, Kanaboshi H, Ikeda K (2000) Isolation of several anti-stress genes from the halotolerant green alga Chlamydomonas by simple functional expression screening with Escherichia coli. World J Microbiol Biotechnol 16:23–29

    Article  CAS  Google Scholar 

  • Moheimani NR (2016) Tetraselmis suecica culture for CO2 bioremediation of untreated flue gas from a coal-fired power station. J Appl Phycol 28:2139–2146

    Article  CAS  Google Scholar 

  • Muller-Feuga A (2004) Microalgae for aquaculture: the current global situation and future trends. In: Richmond A (eds) Handbook of Microalgal Culture. Oxford, Blackwell, pp. 352–364

  • Nikaido I, Asamizu E, Nakajima M, Nakamura Y, Saga N, Tabata S (2000) Generation of 10,154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Res 7:223–227

    Article  PubMed  Google Scholar 

  • Norris RE, Hori T, Floyd GL (1980) Revision of the genus Tetraselmis (class Prasinophyceae). Bot Mag 93:317–339

    Article  Google Scholar 

  • Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E et al (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci U S A 104:7705–7710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Panchuk II, Volkov RA, Schoffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Patron NJ, Waller RF, Archibald JM, Keeling PJ (2005) Complex protein targeting to dinoflagellate plastids. J Mol Biol 348:1015–1024

    Article  PubMed  CAS  Google Scholar 

  • Patron NJ, Waller RF, Keeling PJ (2006) A tertiary plastid uses genes from two endosymbionts. J Mol Biol 357:1373–1382

    Article  PubMed  CAS  Google Scholar 

  • Petersen J, Teich R, Becker B, Cerff R, Brinkmann H (2006) The GapA/B gene duplication marks the origin of Streptophyta (charophytes and land plants). Mol Biol Evol 23:1109–1118

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 9:e45

    Article  Google Scholar 

  • Planelló R, Martinez-Guitarte JL, Morcillo G (2008) The endocrine disruptor bisphenol A increases the expression of HSP70 and ecdysone receptor genes in the aquatic larvae of Chironomus riparius. Chemosphere 71:1870–1876

    Article  PubMed  CAS  Google Scholar 

  • Ponmani T, Guo R, Ki JS (2015) A novel cyclophilin gene from the dinoflagellate Prorocentrum minimum and its possible role in the environmental stress response. Chemosphere 139:260–267

  • Ponmani T, Guo R, Ki JS (2016) Analysis of the genomic DNA of the harmful dinoflagellate Prorocentrum minimum: a brief survey focused on the noncoding RNA gene sequences. J Appl Phycol 28:335–344

    Article  CAS  Google Scholar 

  • Probst AJ, Ladd B, Jarett JK, Geller-McGrath DE, Sieber CMK, Emerson JB, Anantharaman K, Thomas BC et al (2018) Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat Microbiol 3:328–336

    Article  PubMed  CAS  Google Scholar 

  • Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K (2014) Oxidative stress, prooxidants, and antioxidants: the interplay. BioMed Res Int Article ID 761264:1–19

    Google Scholar 

  • Reid AJ, Blake DP, Ansari HR, Billington K, Browne HP, Bryant J, Dunn M, Hung SS, Kawahara F et al (2014) Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Res 24:1676–1685

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Riquelme CE, Avendaño-Herrera R (2003) Microalgae and bacteria interaction in the aquatic environment and their potential use in aquaculture. Rev Chil Hist Nat 76:725–736

    Article  Google Scholar 

  • Rosic NN, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O (2011) Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chaperon 16:69–80

    Article  CAS  Google Scholar 

  • Sathasivam R, Ki JS (2018) A review of the biological activities of microalgal carotenoids and their potential use in healthcare and cosmetic industries. Mar Drugs 16:26

    Article  PubMed Central  Google Scholar 

  • Sathasivam R, Ebenezer V, Guo R, Ki JS (2016) Physiological and biochemical responses of the freshwater green algae Closterium ehrenbergii to the common disinfectant chlorine. Ecotox Environ Safe 133:501–508

    Article  CAS  Google Scholar 

  • Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114

    PubMed  CAS  Google Scholar 

  • Shao ZT, Cong X, Yuan JD, Yang GW, Chen Y, Pan J, An LG (2009) Construction and characterization of a cDNA library from head kidney of Japanese sea bass (Lateolabrax japonicus). Mol Biol Rep 36:2031–2037

    Article  PubMed  CAS  Google Scholar 

  • Shen Y, Liu Y, Liu L, Liang C, Li QQ (2008) Unique features of nuclear mRNA poly(A) signals and alternative polyadenylation in Chlamydomonas reinhardtii. Genetics 179:167–176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shrager J, Hauser C, Chang CW, Harris EH, Davies J, McDermott J, Tamse R, Zhang ZD, Grossman AR (2003) Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information. Plant Physiol 131:401–408

    Article  PubMed  PubMed Central  Google Scholar 

  • Skennerton CT, Ward LM, Michel A, Metcalfe K, Valiente C, Mullin S, Chan KY, Gradinaru V, Orphan VJ (2015) Genomic reconstruction of an uncultured hydrothermal vent gammaproteobacterial methanotroph (family Methylothermaceae) indicates multiple adaptations to oxygen limitation. Front Microbiol 6:1425

    Article  PubMed  PubMed Central  Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Tanaka T, Maeda Y, Veluchamy A, Tanaka M, Abida H, Maréchal E, Bowler C, Muto M, Sunaga Y, Tanaka M, Yoshino T, Taniguchi T, Fukuda Y, Nemoto M, Matsumoto M, Wong PS, Aburatani S, Fujibuchi W (2015) Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. Plant Cell 27:162–176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tredici MR, Biondi N, Ponis E, Rodolfi L, Zittelli GC (2009) Advances in microalgal culture for aquaculture feed and other uses. In: Burnell G, Allan G (eds) New technologies in aquaculture: Improving production efficiency, Quality and environmental management, Cambridge, pp 611–676

  • Tully BJ, Wheat CG, Glazer BT, Huber JA (2018) A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. ISME J 12:1–16

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2015) Dynamic evolution of the chloroplast genome in the green algal classes Pedinophyceae and Trebouxiophyceae. Genome Biol Evol 7:2062–2082

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Utting SD (1985) Influence of nitrogen availability on the biochemical composition of three unicellular marine algae of commercial importance. Aquac Eng 4:175–190

    Article  Google Scholar 

  • Vaquero I, Ruiz-Dominguez MC, Marquez M, Vilchez C (2012) Cu-mediated biomass productivity enhancement and lutein enrichment of the novel microalga Coccomyxa onubensis. Process Biochem 47:694–700

    Article  CAS  Google Scholar 

  • Vizcaíno AJ, Saéz MI, López G, Arizcun M, Abellán E, Martínez TF, Cerón-García MC, Alarcón FJ (2016) Tetraselmis suecia and Tisochrysis lutea meal as dietary ingredients for gilthead sea bream (Sparus aurata L.) fry. J Appl Phycol 28:2843–2855

    Article  CAS  Google Scholar 

  • Worden AZ, Lee JH, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E et al (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Nagarajan H, Lewis NE, Pan S, Cai Z, Liu X, Chen W, Xie M, Wang W, Hammond S, Andersen MR, Neff N, Passarelli B, Koh W, Fan HC, Wang J, Gui Y, Lee KH, Betenbaugh MJ, Quake SR, Famili I, Palsson BO, Wang J (2011) The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nat Biotechnol 29:735–741

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang RY, Li HT, Zhu H, Zhou GP, Wang M, Wang L (2012) Genome sequence of the Trichosporon asahii environmental strain CBS 8904. Eukaryot Cell 11:1586–1587

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang H, Hou Y, Miranda L, Campbell DA, Sturm NR, Gaasterland T, Lin S (2007) Spliced leader RNA trans-splicing in dinoflagellates. Proc Natl Acad Sci U S A 104:4618–4623

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao R, Cao Y, Xu H, Lv L, Qiao D, Cao Y (2011) Analysis of expressed sequence tags from the green alga Dunaliella salina (Chlorophyta). J Phycol 47:1454–1460

  • Zhao S, Xie P, Li G, Jun C, Cai Y, Xiong Q, Zhao Y (2012) The proteomic study on cellular responses of the testes of zebrafish (Danio rerio) exposed to microcystin-RR. Proteomics 12:300–312

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Research Foundation of Korea Grant funded by the Korean Government (2015M1A5A1041805 and 2016R1D1A1A09920198) and by a grant from the National Institute of Fisheries Science, Korea (R2018043) funded to J.-S. Ki.

Author information

Author notes

  1. Jang-Seu Ki

    Present address: Scripps Institution of Oceanography, University of California San Diego, San Diego, CA, 92037, USA

  2. Ramaraj Sathasivam and Ruoyu Guo contributed equally to this work.

Authors and Affiliations

  1. Department of Biotechnology, Sangmyung University, Seoul, 03016, South Korea

    Ramaraj Sathasivam, Ruoyu Guo, Hui Wang & Jang-Seu Ki

  2. Ocean Climate and Ecology Research Division, National Institute of Fisheries Science (NIFS), Busan, 46083, South Korea

    Weol-Ae Lim

Authors
  1. Ramaraj Sathasivam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruoyu Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weol-Ae Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jang-Seu Ki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jang-Seu Ki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sathasivam, R., Guo, R., Wang, H. et al. Expressed sequence tag library of the marine green alga Tetraselmis suecica: a focus on stress-related genes for marine pollution. J Appl Phycol 30, 2387–2402 (2018). https://doi.org/10.1007/s10811-018-1445-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1445-y

Keywords

Search

Navigation