Skip to main content
Log in

Photosynthetic and biochemical responses of the freshwater green algae Closterium ehrenbergii Meneghini (Conjugatophyceae) exposed to the metal coppers and its implication for toxicity testing

  • Microbial Physiology and Biochemistry
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

The freshwater green algae Closterium is sensitive to water quality, and hence has been suggested as ideal organisms for toxicity testing. In the present study, we evaluated the photosynthetic and biochemical responses of C. ehrenbergii to the common contaminants, coppers. The 72 h median effective concentrations (EC50) of CuSO4 and CuCl2 on the test organism were calculated to be 0.202 mg/L and 0.245 mg/L, respectively. Exposure to both coppers considerably decreased pigment levels and photosynthetic efficiency, while inducing the generation of reactive oxygen species (ROS) in cells with increased exposure time. Moreover, the coppers significantly increased the levels of lipid peroxidation and superoxide dismutase (SOD) activity, even at relatively lower concentrations. These suggest that copper contaminants may exert deleterious effects on the photosynthesis and cellular oxidative stress of C. ehrenbergii, representing its powerful potential in aquatic toxicity assessments.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Assche, F.V. and Clijsters, H. 1990. Effects of metals on enzyme activity in plants. Plant Cell Environ. 13, 195–206.

    Article  Google Scholar 

  • Azooz, M.M., Abou-Elhamd, M.F., and Al-Fredan, M.A. 2012. Biphasic effect of copper on growth, proline, lipid peroxidation and antioxidant enzyme activities of wheat (Triticum aestivum cv. Hasaawi) at early growing stage. J. Crop. Sci. 6, 688–694.

    CAS  Google Scholar 

  • Beauchamp, C. and Fridovich, I. 1971. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels.0 Anal. Biochem. 44, 276–287.

    CAS  Google Scholar 

  • Blaylock, B.G., Frank, M.L., and McCarthy, J.F. 1985. Comparative toxicity of copper and acridine to fish, Daphnia and algae. Environ. Toxicol. Chem. 4, 63–67.

    Article  CAS  Google Scholar 

  • Chen, H., Chen, J., Guo, Y., Wen, Y., Liu, J., and Liu, W. 2012. Evaluation of the role of the glutathione redox cycle in Cu (II) toxicity to green algae by a chiral perturbation approach. Aquat. Toxicol. 120–121, 19–26.

    Article  PubMed  CAS  Google Scholar 

  • Cypaite, A., Žaltauskait, J., and Venclovien, J. 2014. The 9th conference environmental engineering. Selected Papers, Article number: enviro.2014.009.

    Google Scholar 

  • Danilov, R.A. and Ekelund, N.G.A. 2001. Responses of photosynthetic efficiency, cell shape and motility in Euglena gracilis (Euglenophyceae) to short-term exposure to heavy metals and pentachlorophenol. Water Air Soil Pollut. 132, 61–73.

    Article  CAS  Google Scholar 

  • Devi, Y.M. and Mehta, S.K. 2014. Changes in antioxidative enzymes of cyanobacterium Nostoc muscorum under copper (Cu2+) stress. Sci. Vision 14, 207–214.

    Article  Google Scholar 

  • Ebenezer, V. and Ki, J.S. 2012. Evaluation of the sub-lethal toxicity of Cu, Pb, bisphenol A and polychlorinated biphenyl to the marine dinoflagellate Cochlodinium polykrikoides. Algae 27, 63–70.

    Article  CAS  Google Scholar 

  • Ebenezer, V. and Ki, J.S. 2013. Quantification of the sub-lethal toxicity of metals and endocrine-disrupting chemicals to the marine green microalga Tetraselmis suecica. Fish. Aquat. Sci. 16, 1–8.

    Google Scholar 

  • Ebenezer, V., Lim, W.A., and Ki, J.S. 2014. Effects of the algicides CuSO4 and NaOCl on various physiological parameters in the harmful dinoflagellate Cochlodinium polykrikoides. J. Appl. Phycol. 26, 2357–2365.

    Article  CAS  Google Scholar 

  • Fukumoto, R.H., Fujii, T., and Sekimoto, H. 1997. Detection and evaluation of a novel sexual pheromone that induces sexual cell division of Closterium ehrenbergii (Chlorophyta). J. Phycol. 33, 441–445.

    Article  CAS  Google Scholar 

  • Gaetke, L.M. and Chow, C.K. 2003. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189, 147–163.

    Article  PubMed  CAS  Google Scholar 

  • Gibbon-Walsh, K., Salaün, P., and van den Berg, C.M. 2012. Pseudopolarography of copper complexes in seawater using a vibrating gold microwire electrode. J. Phys. Chem. A116, 6609–6620.

    Article  CAS  Google Scholar 

  • Guo, R., Lim, W.A., and Ki, J.S. 2016. 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 

  • Heath, R.L. and Packer, L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125, 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Ichimura, T. and Kasai, F. 1984. Post-zygotic isolation between allopatric mating groups of Closterium ehrenbergii Meneghini (Conjugatophyceae). Phycologia 23, 77–85.

    Article  Google Scholar 

  • Ivorra, N., Kraak, M.H.S., and Admiraal, W. 1995. Use of lake water in testing copper toxicity to desmid species. Water Res. 29, 2113–2117.

    Article  CAS  Google Scholar 

  • Kagalou, I., Perdikaris, C., and Petridis, D. 2002. Effects of copper and lead on microalgae (Isochrysis galbana) growth. Fresen. Environ. Bull. 11, 233–236.

    CAS  Google Scholar 

  • Karimi, P., Khavari-Nejad, R.A., Niknam, V., Ghahremaninejad, F., and Najafi, F. 2012. The effects of excess copper on antioxidative enzymes, lipid peroxidation, proline, chlorophyll, and concentration of Mn, Fe, and Cu in Astragalus neo-mobayenii. Sci. World J. 2012, 615670.

    CAS  Google Scholar 

  • Kebeish, R., El-Ayouty, Y., and Husain, A. 2014. Effect of copper on growth, bioactive metabolites, antioxidant enzymes and photosynthesis- related gene transcription in Chlorella vulgaris. World J. Biol. Biol. Sci. 2, 34–43.

    Google Scholar 

  • Ken, C.F., Hsiumg, T.M., Huang, Z.X., Juang, R.H., and Lin, C.T. 2005. Characterization of the Fe/Mn-superoxide dismutase from diatom (Thallassiosira weissflogii): cloning, expression and property. J. Agr. Food. Chem. 53, 1470–1474.

    Article  CAS  Google Scholar 

  • Kim, S.G., Matsui, S., and Hamada, J. 1998. Toxicity test of anionic and nonionic surfactants to Closterium ehrenbergii by new indexes. J. Environ. Conserv. Eng. 27, 274–281.

    Article  CAS  Google Scholar 

  • Knauer, K., Behra, R., and Sigg, L. 1997. Effects of free Cu2+ and Zn2+ ions on growth and metal accumulation in fresh-water algae. Environ. Toxicol. Chem. 16, 220–229.

    Article  CAS  Google Scholar 

  • Knauert, S. and Knauer, K. 2008. The role of reactive oxygen species in copper toxicity to two freshwater green algae. J. Phycol. 44, 311–319.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, M., Kakizono, T., Nishio, N., Nagai, S., Kurimura, Y., and Tsuji, Y. 1997. Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Appl. Microbiol. Biotechnol. 48, 351–356.

    Article  CAS  Google Scholar 

  • Lee, M.A., Guo, R., Ebenezer, V., and Ki, J.S. 2015. Evaluation and selection of reference genes for ecotoxicogenomic study of the green alga Closterium ehrenbergii using quantitative real-time PCR. Ecotoxicology 24, 863–872.

    Article  PubMed  CAS  Google Scholar 

  • Lee, M.A., Guo, R., and Ki, J.S. 2014. Different transcriptional responses of heat shock protein 20 in the marine diatom Ditylum brightwellii exposed to metals and endocrine-disrupting chemicals. Environ. Toxicol. 29, 1379–1389.

    Article  PubMed  CAS  Google Scholar 

  • Li, M., Hu, C., Zhu, Q., Chen, L., Kong, Z., and Liu, Z. 2006. Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62, 565–572.

    Article  PubMed  CAS  Google Scholar 

  • Ma, M., Zhu, W., Wang, Z., and Witkamp, G.J. 2003. Accumulation, assimilation and growth inhibition of copper on freshwater alga (Scenedesmus subspicatus 86.81 SAG) in the presence of EDTA and fulvic acid. Aquat. Toxicol. 63, 221–228.

    Article  PubMed  CAS  Google Scholar 

  • Magdaleno, A., Vélez, C.G., Wenzel, M.T., and Tell, G. 2013. Effects of cadmium, copper and zinc on growth of four isolated algae from a highly polluted Argentina river. Bull. Environ. Contam. Toxicol. 92, 202–207.

    Article  PubMed  CAS  Google Scholar 

  • Mamboya, F.A., Pratap, H.B., Mtolera, M., and Björk, M. 1999. The effect of copper on the daily growth rate and photosynthetic efficiency of the brown macroalga Padina boergesenii, pp. 185–192. Proceedings of the 20th anniversary conference on advances on marine sciences in Tanzania, IMS, Zanzibar (Tanzania).

    Google Scholar 

  • Marshall, J.A. and Newman, S. 2002. Differences in photoprotective pigment production between Japanese and Australian strain of Chattonella marina (Raphidophyeeae). J. Exp. Mar. Biol. Ecol. 272, 13–27.

    Article  CAS  Google Scholar 

  • Mishra, S., Jha, A.B., and Dubey, R.S. 2011. Arsenite treatment induces oxidative stress, upregulates antoxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248, 565–577.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405–410.

    Article  PubMed  CAS  Google Scholar 

  • Organization for Economic Cooperation and Development (OECD). 2011. OECD guidelines for the testing of chemicals. Freshwater algal and cyanobacteria growth inhibition test. 201. OECD Publications, Paris, France.

  • Parsons, T.R., Maita, Y., and Lalli, C.M. 1984. A manual of chemical and biological methods for seawater analysis. Pergamon press, Oxford, UK.

    Google Scholar 

  • Peng, C.C., Chyau, C.C., Wang, H.E., Chang, H.C., Chen, K.C., Chou, K.Y., and Peng, R.Y. 2013. Cytotoxicity of ferulic acid on T24 cell line differentiated by different microenvironments. Biomed Res. Int. 2013, 579859.

    PubMed  PubMed Central  Google Scholar 

  • Penuelas, J. and Filella, I. 2002. Metal pollution in Spanish terrestrial ecosystems during the twentieth century. Chemosphere 46, 501–505.

    Article  PubMed  CAS  Google Scholar 

  • Pinto, E., Carvalho, A.P., Cardozo, K.H.M., Malcata, F.X., Fabyana, M.A., and 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. Farmacogn. 21, 349–354.

    Article  CAS  Google Scholar 

  • Qin, Y., Lu, M., and Gong, X. 2008. Dihydrorhodamine 123 is superior to 2,7-dichlorodihydrofluorescein diacetate and dihydrorhodamine 6G in detecting intracellular hydrogen peroxide in tumor cells. Cell Biol. Int. 32, 224–228.

    Article  PubMed  CAS  Google Scholar 

  • Rachlin, J.W., Jensen, T.E., and Warkentim, B. 1983. The growth response of the diatom Navicula incerta to selected concentrations of the metals: cadmium, copper, lead and zinc. Bull. Torrey Bot. Club 110, 217–223.

    Article  CAS  Google Scholar 

  • Sarthou, G., Timmermans, K.R., Blain, S., and Tréguer, P. 2005. Growth physiology and fate of diatoms in the ocean: a review. J. Sea Res. 53, 25–42.

    Article  CAS  Google Scholar 

  • Sathasivam, R., Ebenezer, V., Guo, R., and Ki, J.S. 2016. Physiological and biochemical responses of the freshwater green algae Closterium ehrenbergii to the common disinfectant chlorine. Ecotoxicol. Environ. Saf. 133, 501–508.

    Article  PubMed  CAS  Google Scholar 

  • Sbihi, K., Cherifi, O., El gharmali, A., Oudra, B., and Aziz, F. 2012. Accumulation and toxicological effects of cadmium, copper and zinc on the growth and photosynthesis of the freshwater diatom Planothidium lanceolatum (Brébisson) Lange-Bertalot: A laboratory study. J. Mater. Environ. Sci. 3, 497–506.

    CAS  Google Scholar 

  • Schreiber, U., Hormann, H., Neubauer, C., and Klughammer, C. 1995. Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. J. Plant Physiol. 22, 209–220.

    CAS  Google Scholar 

  • Sharma, P., Jha, A.B., Dubey, R.S., and Pessarakli, M. 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful condition. Am. J. Bot. 2012, 217037.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Soto, P., Gaete, H., and Hidalgo, M.E. 2011. Assessment of catalase activity, lipid peroxidation, chlorophyll-a and growth rate in the freshwater green algae Pseudokirchneriella subcapitata exposed to copper and zinc. Lat. Am. J. Aquat. Res. 39, 280–285.

    Article  Google Scholar 

  • Spickett, C.M., Jerlich, A., Panasenko, O.M., Arnhold, J., Pitt, A.R., Stelmaszynska, T., and Schaur, R.J. 2000. The reactions of hypochlorous acid, the reactive oxygen species produced by myeloperoxidase, with lipids. Acta Biochim. Pol. 47, 889–899.

    PubMed  CAS  Google Scholar 

  • Suzelei, R., Gaeta, E.E.L., Fonseca, S.F.C., and Emanuele, T.A. 2012. Cadmium and chromium toxicity to Pseudokirchneriella subcapitata and Microcystis aeruginosa. Braz. Arch. Biol. Technol. 55, 161–169.

    Article  CAS  Google Scholar 

  • Teisseyre, A. and Mozrzymas, J.W. 2006. The inhibitory effect of copper ions on lymphocyte Kv1.3 potassium channels. J. Physiol. Pharmacol. 57, 301–314.

    PubMed  CAS  Google Scholar 

  • Viana, S.M. and Rocha, O. 2005. The toxicity of copper sulphate and atrazine to the diatom Aulacoseira granulata (Ehrenberg) Simmons. Acta Limnol. Bras. 17, 291–300.

    Google Scholar 

  • Wang, Z.H., Nie, X.P., Yue, W.J., and Li, X. 2012. Physiological responses of three marine microalgae exposed to cypermethrin. Environ. Toxicol. 27, 563–572.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H., Sathasivam, R., and Ki, J.S. 2017. Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments. Algae 32, 131–137.

    Article  Google Scholar 

  • Watanabe, M.M., Kawachi, M., Hiroki, M., and Kasai, F. 2000. NIEScollection list of strains, p. 159. 6th ed., 2000 microalgae and protozoa. Microbial culture collections, National institute for environmental studies, Tsukuba, Japan.

    Google Scholar 

  • Yan, H. and Pan, G. 2002. Toxicity and bioaccumulation of copper in three green microalgal species. Chemosphere 49, 471–476.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

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

Wang, H., Ebenezer, V. & Ki, JS. Photosynthetic and biochemical responses of the freshwater green algae Closterium ehrenbergii Meneghini (Conjugatophyceae) exposed to the metal coppers and its implication for toxicity testing. J Microbiol. 56, 426–434 (2018). https://doi.org/10.1007/s12275-018-8081-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-018-8081-8

Keywords

Navigation