Skip to main content

Gracilaria tenuistipitata (Rhodophyta) tolerance to cadmium and copper exposure observed through gene expression and photosynthesis analyses

Journal of Applied Phycology volume 30, pages 2129–2141 (2018)Cite this article

Abstract

Heavy metals are toxic to all organisms and their presence can have great impact on ecosystems. The study of strategies to remove contaminants is thus important, as is increased understanding of the resistance mechanisms of candidate organisms to be used as phytoremediators. The present study evaluate the genes involved in chronic stress using two different expression techniques to profile the transcriptome of the marine macroalga Gracilaria tenuistipitata after exposure to the EC50 of cadmium (Cd) and copper (Cu). Some known molecular markers for chronic pollution were observed, indicating that resistance mechanisms are induced within the first hour of treatment. Differences in gene expression response patterns between the two metals were found, where Cd up-regulated the expressions of superoxide dismutase and the nitrate transporter NRT even after 6 days of exposure. Expressions of both nuclear and chloroplast-encoded proteins were affected, and a stronger tolerance mechanism involving proteins of unknown function is certainly connected to the tolerance of the alga, warranting further studies. After 6 days of exposure to Cd or Cu, a slower acclimation was detected for the latter. Analysis of the photosynthetic rate revealed acclimation over time, corroborating a previous study where G. tenuistipitata was able to accumulate these metals and tolerate their negative effects, reinforcing the potential use of this macroalga in integrated bioremediation processes.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Abreu MH, Varela DA, Henriquez L, Villarroel A, Yarish C, Sousa-Pinto I, Buschmann AH (2009) Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis. Aquaculture 293:211–220

    Article  Google Scholar 

  • Aitken D, Bulboa C, Godoy-Faundez A, Turrion-Gomez JL, Antizar-Ladislao B (2014) Life cycle assessment of macroalgae cultivation and processing for biofuel production. J Clean Prod 75:45–56

    Article  CAS  Google Scholar 

  • Andrade LR, Farina M, Filho GMA (2004) Effects of copper on Enteromorpha flexuosa (Chlorophyta) in vitro. Ecotoxicol Environ Saf 58:117–125

    Article  PubMed  CAS  Google Scholar 

  • Andrade S, Pulido MJ, Correa JA (2010) The effect of organic ligands exuded by intertidal seaweeds on copper complexation. Chemosphere 78:397–401

    Article  PubMed  CAS  Google Scholar 

  • Arnér ESJ, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109

    Article  PubMed  Google Scholar 

  • Barufi JB, Oliveira EC, Plastino EM, Oliveira MC (2010) Life history, morphological variability and growth rates of life phases of Gracilaria tenuistipitata (Gracilariales, Rhodophyta) in vitro. Sci Mar 74:297–303

    Article  Google Scholar 

  • Bellorin AM, Oliveira MC, Oliveira EC (2002) Phylogeny and systematics of the marine algal family Gracilariaceae (Gracilariales, Rhodophyta) based on small subunit rDNA and its sequences of Atlantic and Pacific species. J Phycol 38:551–563

    Article  CAS  Google Scholar 

  • Bezerra AF, Marinho-Soriano E (2010) Cultivation of the red seaweed Gracilaria birdiae (Gracilariales, Rhodophyta) in tropical waters of northeast Brazil. Biomass Bioenergy 34:1813–1817

    Article  Google Scholar 

  • Bossuyt BTA, Janssen CR (2004) Long-term acclimation of Pseudokirchneriella subcapitata (Korshikov) Hindak to different copper concentrations: changes in tolerance and physiology. Aquat Toxicol 68:61–74

    Article  PubMed  CAS  Google Scholar 

  • Brown MT, Depledge MH (1998) Determinants of trace metal concentrations in marine organisms. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environments. Chapman and Hall, London, pp 185–217

    Chapter  Google Scholar 

  • Cardozo KH, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C 146:60–78

    Article  CAS  Google Scholar 

  • Chen Y, Lin L, Viadero RC, Gang D (2007) Nonpoint source pollution. Water Environ Res 79:2032–2048

    Article  CAS  Google Scholar 

  • Chrispeels MJ, Crawford NM, Schroeder JI (1999) Proteins for transport of water and mineral nutrients across the membranes of plant cells. Plant Cell 11:661–675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  PubMed  CAS  Google Scholar 

  • Collén Nyvall P, Collén J, Reis MS, Pedersén M, Setubal JC, Varani AM, Colepicolo P, Oliveira MC (2012) Analysis of expressed sequence tags from the agarophyte Gracilaria tenuistipitata (Rhodophyta). J Appl Phycol 24:641–647

    Article  CAS  Google Scholar 

  • Collén J, Pinto E, Pedersén M, Colepicolo P (2003) Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Arch Environ Contam Toxicol 45(3):337–342

    Article  PubMed  CAS  Google Scholar 

  • Contreras-Porcia L, Dennett G, González A, Vergara E, Medina C, Correa JA, Moenne A (2011) Identification of copper-induced genes in the marine alga Ulva compressa (Chlorophyta). Mar Biotechnol 13:544–556

    Article  PubMed  CAS  Google Scholar 

  • Cortez DA, Tonon AP, Colepicolo P, Vêncio RZ (2011) Combining P values to improve classification of differential gene expression in the HTself software. Genet Mol Res 10:3586–3595

    Article  PubMed  CAS  Google Scholar 

  • Critchley AT (1993) Gracilaria (Rhodophyta, Gracilariales): an economically important agarophyte. In: Ohno M, Critchley AT (eds) Seaweed cultivation and marine ranching. JICA, Yokosuka, pp 89–112

    Google Scholar 

  • Edwards P (1970) Illustrated guide to seaweeds and seagrasses in the vicinity of Porto Aransas, Texas. Contrib Mar Sci 15:1–228

    Google Scholar 

  • Falcão VR, Oliveira MC, Colepicolo P (2010) Molecular characterization of nitrate reductase gene and its expression in the marine red alga Gracilaria tenuistipitata (Rhodophyta). J Appl Phycol 22:613–622

    Article  CAS  Google Scholar 

  • Gerlach AS (1981) Marine pollution: diagnosis and therapy. Springer-Verlag, Berlin, p 218

    Book  Google Scholar 

  • Gledhill M, Nimmo M, Hill SJ, Brown MT (1997) The toxicity of copper (II) species to marine algae, with particular reference to macroalgae. J Phycol 33:2–11

    Article  CAS  Google Scholar 

  • Gressler V, Fujii MT, Martins AP, Colepicolo P, Pinto E (2011) Biochemical composition of two red seaweed species grown on the Brazilian coast. J Sci Food Agric 91:1687–1692

    Article  PubMed  CAS  Google Scholar 

  • Gribble GW (1999) The diversity of naturally occurring organobromine compounds. Chem Soc Rev 28:335–346

    Article  CAS  Google Scholar 

  • Guillemin ML, Faugeron S, Destombe C, Viard F, Correa JA, Valero M (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution 62:1500–1519

    Article  PubMed  Google Scholar 

  • Haglund K, Björk M, Ramazanov Z, García-Reina G, Pedersén M (1992) Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187:275–281

    Article  PubMed  CAS  Google Scholar 

  • Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, Oliveira MC (2004) Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights on the evolution of rhodoplasts and their relationship to other plastids. J Mol Evol 59:464–477

    Article  PubMed  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • Han BP, Virtanen M, Koponen J, Straskraba M (2000) Effect of photoinhibition on algal photosynthesis: a dynamic model. J Plankton Res 22:865–885

    Article  CAS  Google Scholar 

  • Han T, Kang SH, Park JS, Lee HK, Brown MT (2008) Physiological responses of Ulva pertusa and U. armoricana to copper exposure. Aquat Toxicol 86:176–184

    Article  PubMed  CAS  Google Scholar 

  • Herrero R, Lodeiro P, Rojo R, Ciorba A, Rodríguez P, Sastre de Vicente ME (2008) The efficiency of the red alga Mastocarpus stellatus for remediation of cadmium pollution. Bioresour Technol 99:4138–4146

    Article  PubMed  CAS  Google Scholar 

  • Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F, Vigh L (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a “fluidity gene”. Proc Natl Acad Sci U S A 95:3513–3518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hu S, Tang CH, Wu ML (1996) Cadmium accumulation by several seaweeds. Sci Total Environ 187:65–71

    Article  CAS  Google Scholar 

  • Huang X, Ke CH, Wang WX (2010) Cadmium and copper accumulation and toxicity in the macroalga Gracilaria tenuistipitata. Aquat Biol 11:17–26

    Article  Google Scholar 

  • Hutchins CM, Simon DF, Zerges W, Wilkinson KJ (2010) Transcriptomic signatures in Chlamydomonas reinhardtii as Cd biomarkers in metal mixtures. Aquat Toxicol 100:120–127

  • Ishida K, Green BR (2002) Second and third-hand chloroplasts in dinoflagellates: phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proc Natl Acad Sci U S A 99:9294–9299

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jegerschold C, Arellano JB, Schroder WP, Vankan PJM, Baron M, Styring S (1995) Copper (II) inhibition of electron-transfer through photosystem-II studied by EPR spectroscopy Biochemistry 34:12747–12754

  • Jez JM, Cahoon RE, Chen S (2004) Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J Biol Chem 279:33463–33470

    Article  PubMed  CAS  Google Scholar 

  • Juwarkar AA, Singh SK, Mudhoo A (2010) A comprehensive overview of elements in bioremediation. Rev Environ Sci Biotechnol 9:215–288

    Article  CAS  Google Scholar 

  • Kaneko K, Washio K, Umezawa T, Matsuda F, Morikawa M, Okino T (2014) cDNA cloning and characterization of vanadium-dependent bromoperoxidases from the red alga Laurencia nipponica. Biosci Biotechnol Biochem 78:1310–1319

    Article  PubMed  CAS  Google Scholar 

  • Kidgell JT, de Nys R, Paul NA, Roberts DA (2014) The sequential application of macroalgal biosorbents for the bioremediation of a complex industrial effluent. PLoS One 9(8):e106375

    Article  CAS  Google Scholar 

  • Kolber Z, Falkowski P G (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in-situ. Limnol Oceanogr 38: 1646–1665

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar KS, Dahms HU, Won EJ, Lee JS, Shin KH (2015) Microalgae—a promising tool for heavy metal remediation. Ecotoxicol Environ Saf 113:329–352

    Article  CAS  Google Scholar 

  • Kupper H, Setlik I, Spiller M, Kupper FC, Prasil O (2002) Heavy metal-induced inhibition of photosynthesis: Targets of in vivo heavy metal chlorophyll formation J Phycol 38:429–441

  • Lambert AS, Morin S, Artigas J, Volat B, Coquery M, Neyra M, Pesce S (2012) Structural and functional recovery of microbial biofilms after a decrease in copper exposure: influence of the presence of pristine communities. Aquat Toxicol 109:118–126

    Article  PubMed  CAS  Google Scholar 

  • Laporte D, Valdes N, Gonzalez A, Saez CA, Zuniga A, Navarrete A, Meneses C, Moenne A (2016) Copper-induced overexpression of genes encoding antioxidant system enzymes and metallothioneins involve the activation of CaMs, CDPKs and MEK1/2 in the marine alga Ulva compressa. Aquat Toxicol 177:433–440

    Article  PubMed  CAS  Google Scholar 

  • Lawton RJ, Rebecca J, Mata L, de Nys R, Paul NA (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS One 8(10):e0077344

    Article  CAS  Google Scholar 

  • Lee TM, Chang YC (1999) An increase of ornithine delta-aminotransferase-mediated proline synthesis in relation to high-temperature injury in Gracilaria tenuistipitata (Gigartinales, Rhodophyta). J Phycol 35:84–88

    Article  Google Scholar 

  • Lee Y C, Chang S P (2011) The biosorption of heavy metals from aqueous solution by Spirogyra and Cladophora filamentous macroalgae. Bioresour Technol 102: 5297–5304

  • Lemaire S, Keryer E, Stein M, Schepens I, Issakidis-Bourguet E, Gérard-Hirne C, Miginiac-Maslow M, Jacquot JP (1999) Heavy-metal regulation of thioredoxin gene expression in Chlamydomonas reinhardtii. Plant Physiol 120:773–778

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leusch A, Volesky B (1995) The influence of film diffusion on cadmium biosorption by marine biomass. J Biotechnol 43:1–10

    Article  CAS  Google Scholar 

  • Levy JL, Angel BM, Stauber JL, Poon WL, Simpson SL, Cheng SH, Jolley DF (2008) Uptake and internalization of copper by three marine microalgae: comparison of copper-sensitive and copper-tolerant species. Aquat Toxicol 89:82–93

    Article  PubMed  CAS  Google Scholar 

  • Liu QY, Baldauf SL, Reith ME (1996) Elongation factor 1 alpha genes of the red alga Porphyra purpurea include a novel, developmentally specialized variant. Plant Mol Biol 31:77–85

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lopes PF, Oliveira MC, Colepicolo P (2002) Daily variation of nitrate reductase activity in the red alga Gracilaria tenuistipitata (Rhodophyta) is due to changes in cellular protein levels. Biochem Biophys Res Commun 295:50–54

    Article  PubMed  CAS  Google Scholar 

  • Lumsden BR, Florence TM (1983) A new algal assay procedure for the determination of the toxicity of copper species in seawater. Environ Technol Lett 4:271–276

    Article  CAS  Google Scholar 

  • Macfie SM, Welbourn PM (2000) The cell wall as a barrier to uptake of metal ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae). Arch Environ Contam Toxicol 39:413–419

    Article  PubMed  CAS  Google Scholar 

  • Mallick N, Rai LC (1994) Kinetic-studies of mineral uptake and enzyme-activities of Anabaena doliolum under metal stress. J Gen Appl Microbiol 40:123–133

    Article  CAS  Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69

  • Marinho-Soriano E (2001) Agar polysaccharides from Gracilaria species (Rhodophyta, Gracilariaceae). J Biotechnol 89:81–84

    Article  PubMed  CAS  Google Scholar 

  • Marinho-Soriano E, Panucci RA, Carneiro MAA, Pereira DC (2009) Evaluation of Gracilaria caudata J. Agardh for bioremediation of nutrients from shrimp farming wastewater. Bioresour Technol 100:6192–6198

    Article  PubMed  CAS  Google Scholar 

  • Martins AP, Yokoya NS, Colepicolo P (2016) Biochemical modulation by carbon and nitrogen addition in cultures of Dictyota menstrualis (Dictyotales, Phaeophyceae) to generate oil-based bioproducts. Mar Biotechnol 18:314–326

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga T, Takeyama H, Nakao T, Yamazawa A (1999) Screening of marine microalgae for bioremediation of cadmium-polluted seawater. J Biotechnol 70:33–38

    Article  PubMed  CAS  Google Scholar 

  • McHugh DJ (1991) Worldwide distribution of commercial resources of seaweeds including Gelidium. Hydrobiologia 221:9–29

    Article  Google Scholar 

  • Mi HY, Muruganujan A, Casagrande JT, Thomas PD (2013) Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8:1551–1566

    Article  PubMed  CAS  Google Scholar 

  • Miao AJ, Wang WX (2006) Cadmium toxicity to two marine phytoplankton under different nutrient conditions. Aquat Toxicol 78:114–126

    Article  PubMed  CAS  Google Scholar 

  • Moulin P, Andría JR, Axelsson L, Mercado JM (2011) Different mechanisms of inorganic carbon acquisition in red macroalgae (Rhodophyta) revealed by the use of TRIS buffer. Aquat Bot 95:31–38

    Article  CAS  Google Scholar 

  • Murphy V, Hughes H, McLoughlin P (2007) Cu(II) binding by dried biomass of red, green and brown macroalgae. Water Res 41:731–740

    Article  PubMed  CAS  Google Scholar 

  • Najafpour MM, Govindjee (2011) Oxygen evolving complex in photosystem II: better than excellent. Dalton Trans 40:9076–9084

    Article  PubMed  CAS  Google Scholar 

  • Necchi O (2004) Light-related photosynthetic characteristics of lotic macroalgae. Hydrobiologia 525:139–155

    Article  Google Scholar 

  • Nharingo T, Moyo M (2016) Application of Opuntia ficus-indica in bioremediation of wastewaters: a critical review. J Environ Manag 166:55–72

    Article  CAS  Google Scholar 

  • Nielsen HD, Nielsen SL (2010) Adaptation to high light irradiances enhances the photosynthetic Cu2+ resistance in Cu2+ tolerant and non-tolerant populations of the brown macroalgae Fucus serratus. Mar Pollut Bull 60:710–717

    Article  PubMed  CAS  Google Scholar 

  • Nielsen HD, Brownlee C, Coelho SM, Brown MT (2003) Inter-population differences in inherited copper tolerance involves photosynthetic adaptation and exclusion mechanisms in Fucus serratus. New Phytol 160:157–165

    Article  CAS  Google Scholar 

  • Nriagu JO, Pacyna JM (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333:134–139

    Article  PubMed  CAS  Google Scholar 

  • Okamoto OK, Shao L, Hastings JW, Colepicolo P (1999) Acute and chronic effects of toxic metals on viability, encystment and bioluminescence in the dinoflagellate Gonyaulax polyedra. Comp Biochem Physiol C 123(1):75–83

    PubMed  CAS  Google Scholar 

  • Oliveira EC, Alveal K (1990) The mariculture of Gracilaria (Rhodophyta) for the production of agar. In: Akatsuka I (ed) Introduction to applied phycology. SBP Academic Publishing, The Hague, pp 553–564

    Google Scholar 

  • Pashalidis S, Moreira LM, Zaini PA, Campanharo JC, Alves LMC, Ciapina LP, Vencio RZN, Lemos EGM, da Silva AM, da Silva ACR (2005) Whole-genome expression profiling of Xylella fastidiosa in response to growth on glucose. OMICS 9:77–90

    Article  PubMed  CAS  Google Scholar 

  • Pawlik-Skowronska B, Pirszel J, Brown MT (2007) Concentrations of phytochelatins and glutathione found in natural assemblages of seaweeds depend on species and metal concentrations of the habitat. Aquat Toxicol 83:190–199

    Article  PubMed  CAS  Google Scholar 

  • Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648

    Article  PubMed  CAS  Google Scholar 

  • Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018

    Article  CAS  Google Scholar 

  • Pinto E, Carvalho AP, Cardozo KHM, Malcata FX, dos Anjos FM, Colepicolo P (2011) Effects of heavy metals and light levels on the biosynthesis of carotenoids and fatty acids in the macroalgae Gracilaria tenuistipitata (var. liui Zhang & Xia). Rev Bras Farm 21:349–354

    Article  CAS  Google Scholar 

  • Platt T, Gallegos CL, Harnson WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Rasband WS (1997–2014) ImageJ, US National Institutes of Health, Bethesda, Maryland. http://rsb.info.nih.gov/ij/

  • Ratkevicius N, Correa JA, Moenne A (2003) Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ 26:1599–1608

    Article  CAS  Google Scholar 

  • Ritter A, Ubertini M, Romac S, Gaillard F, Delage L, Mann A, Cock JM, Tonon T, Correa JA, Potin P (2010) Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics 10:2074–2088

    Article  PubMed  CAS  Google Scholar 

  • Roeder V, Collén J, Rousvoal S, Corre E, Leblanc C, Boyen C (2005) Identification of stress gene transcripts in Laminaria digitata (Phaeophyceae) protoplast cultures by expressed sequence tag analysis. J Phycol 41:1227–1235

    Article  CAS  Google Scholar 

  • Romano RL, Liria CW, Machini MT, Colepicolo P, Zambotti-Villela L (2017) Cadmium decreases the levels of glutathione and enhances the phytochelatin concentration in the marine dinoflagellate Lingulodinium polyedrum. J Appl Phycol 29:811–820

    Article  CAS  Google Scholar 

  • Rowley DA, Halliwell B (1982) Superoxide-dependent formation of hydroxyl radicals from NADH and NADPH in the presence of iron salts. FEBS Lett 142:39–41

    Article  PubMed  CAS  Google Scholar 

  • Saunders RJ, Paul NA, Hu Y, de Nys R (2012) Sustainable sources of biomass for bioremediation of heavy metals in waste water derived from coal-fired power generation. PLoS One 7:e36470

    Article  PubMed  PubMed Central  Google Scholar 

  • Serra A, Guasch H (2009) Effects of chronic copper exposure on fluvial systems: linking structural and physiological changes of fluvial biofilms with the in-stream copper retention. Sci Total Environ 407:5274–5282

    Article  PubMed  CAS  Google Scholar 

  • Sigaud-Kutner TC, Pinto E, Okamoto OK, Latorre LR, Colepicolo P (2002) Changes in superoxide dismutase activity and photosynthetic pigment content during growth of marine phytoplankters in batch-cultures. Physiol Plant 114:566–571

    Article  PubMed  CAS  Google Scholar 

  • Soldo D, Behra R (2000) Long-term effects of copper on the structure of freshwater periphyton communities and their tolerance to copper, zinc, nickel and silver. Aquat Toxicol 47:181–189

    Article  CAS  Google Scholar 

  • Stengel DB, Macken A, Morrison L, Morley N (2004) Zinc concentrations in marine macroalgae and a lichen from western Ireland in relation to phylogenetic grouping, habitat and morphology. Mar Pollut Bull 48:902–909

    Article  PubMed  CAS  Google Scholar 

  • Takahashi MM, Oliveira MC (2011) Sequencing and analysis of the mitochondrial genome of Gracilaria tenuistipitata (Gracilariales, Rhodophyta). J Phycol 47:28–28

    Google Scholar 

  • Tonon AP (2009) Evaluation of genes expression by microarrays in Gracilaria tenuistipitata subjected to stress by heavy metals. PhD Thesis. University of São Paulo

  • Tonon AP, Oliveira MC, Soriano EM, Colepicolo P (2011) Absorption of metals and characterization of chemical elements present in three species of Gracilaria (Gracilariaceae) Greville: a genus of economical importance. Rev Bras Farm 21:355–360

    Article  CAS  Google Scholar 

  • Torres FAE, Passalacqua TG, Velasquez AMA, Souza RA, Colepicolo P, Graminha MAS (2014) New drugs with antiprotozoal activity from marine algae: a review. Rev Bras Farm 24:265–276

    Article  CAS  Google Scholar 

  • Vencio RZ, Koide T (2005) HTself: self-self based statistical test for low replication microarray studies. DNA Res 12:211–214

    Article  PubMed  CAS  Google Scholar 

  • Wang SZ, Zhang DY, Pan XL (2013) Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere 93:230–237

    Article  PubMed  CAS  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    Article  PubMed  CAS  Google Scholar 

  • Winter JM, Moore BS (2009) Exploring the chemistry and biology of vanadium-dependent haloperoxidases. J Biol Chem 284:18577–18581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453–465

    Article  CAS  Google Scholar 

  • Wu HY (2016) Effect of different light qualities on growth, pigment content, chlorophyll fluorescence, and antioxidant enzyme activity in the red alga Pyropia haitanensis (Bangiales, Rhodophyta). Biomed Res Int. https://doi.org/10.1155/2016/7383918

  • Zeng J, Wang W-X (2009) The importance of cellular phosphorus in controlling the uptake and toxicity of cadmium and zinc in Microcystis aeruginosa, a freshwater cyanobacterium. Environ Toxicol Chem 28:1618–1626

  • Zhang W, Li HY (2007) Development of an eco-friendly agar extraction technique from the red seaweed Gracilaria lemaneiformis. J Biotechnol 131:194–195

    Article  Google Scholar 

  • Zhou Y, Yang HS, HY H, Liu Y, Mao YZ, Zhou H, XL X, Zhang FS (2006) Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China. Aquaculture 252:264–276

    Article  Google Scholar 

Download references

Funding

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Centre National de la Recherche Scientifique (CNRS).

Author information

Authors and Affiliations

  1. Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, Brazil

    Angela Pedroso Tonon, Paulo Adriano Zaini, Vanessa dos Reis Falcão & Pio Colepicolo

  2. Department of Botany, Institute of Biosciences, University of São Paulo, São Paulo, Brazil

    Mariana Cabral Oliveira

  3. UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, Sorbonne Universités, UPMC Univ Paris VI, CS 90074, 29688, Roscoff, France

    Jonas Collén & Catherine Boyen

  4. CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, 29688, Roscoff, France

    Jonas Collén & Catherine Boyen

Authors
  1. Angela Pedroso Tonon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Adriano Zaini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vanessa dos Reis Falcão
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mariana Cabral Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jonas Collén
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Catherine Boyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pio Colepicolo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela Pedroso Tonon.

Electronic supplementary material

ESM 1

(DOCX 277 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tonon, A.P., Zaini, P.A., dos Reis Falcão, V. et al. Gracilaria tenuistipitata (Rhodophyta) tolerance to cadmium and copper exposure observed through gene expression and photosynthesis analyses. J Appl Phycol 30, 2129–2141 (2018). https://doi.org/10.1007/s10811-017-1360-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1360-7

Keywords

  • Heavy metals
  • Marine macroalgae
  • Gene expression
  • Stress response