Skip to main content
SpringerLink
Log in

Comparison in copper accumulation and physiological responses of Gracilaria lemaneiformis and G. lichenoides (Rhodophyceae)

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Heavy metal pollution has become a worldwide problem in aquaculture. We studied copper (Cu2+) accumulation and physiological responses of two red algae Gracilaria lemaneiformis and Gracilaria lichenoides from China under Cu2+ exposure of 0–500 μg/L in concentration. Compared with G. lemaneiformis, G. lichenoides was more capable in accumulating Cu2+, specifically, more Cu2+ on extracellular side (cell wall) than on intracellular side (cytoplasm) and in cell organelles (especially chloroplast, cell nucleus, mitochondria, and ribosome). In addition, G. lichenoides contained more insoluble polysaccharide in cell wall, which might promote the extracellular Cu2+-binding as an efficient barrier against metal toxicity. Conversely, G. lemaneiformis was more vulnerable than G. lichenoides to Cu2+ toxin for decreases in growth, pigment (chlorophyll a, chlorophyll b, phycobiliprotein, and β-carotene) content, and photosynthetic activity. Moreover, more serious oxidative damages in G. lemaneiformis than in G. lichenoides, in accumulation of reactive oxidative species and malondialdehyde, and in electrolyte leakage, because of lower antioxidant enzyme (superoxide dismutase and glutathione reductase) activities. Therefore, G. lichenoides was less susceptible to Cu2+ stress than G. lemaneiformis.

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

Similar content being viewed by others

References

  • Andrade L R, Leal R N, Noseda M, Duarte M E, Pereira M S, Mourão P A, Farina M, Amado Filho G M. 2010. Brown algae overproduce cell wall polysaccharides as a protection mechanism against the heavy metal toxicity. Marine Pollution Bulletin, 60(9): 1 482–1 488.

    Article  Google Scholar 

  • Ata A, Nalcaci O O, Ovez B. 2012. Macro algae Gracilaria verrucosa as a biosorbent: A study of sorption mechanisms. Algal Research, 1(2): 194–204.

    Article  Google Scholar 

  • Axelsson B, Axelsson L. 1987. A rapid and reliable method to quantify environmental effects on Laminaria based on measurements of ion leakage. Bot. Mar., 30: 55–61.

    Article  Google Scholar 

  • Bolhar-Nordenkampf H R, Long S P, Baker N R, Oquist G, Schreiber U, Lechner E G. 1989. Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Funct. Ecol. 3: 497–514.

    Article  Google Scholar 

  • Boyd C E, Massaut L. 1999. Risk associated with the use of chemicals in pond aquaculture. Aquac. Eng., 20: 113–132.

    Article  Google Scholar 

  • Brooks R R, Shaw S, Marfil A A. 1981. The chemical form and physiological function of nickel in some Iberian Alyssum species. Physiol. Plant, 51: 167–170.

    Article  Google Scholar 

  • Brown M T, Newman J E. 2003. Physiological responses of Gracilariopsis longissima (S. G. Gmelin) Steentoft L M Irvine and Farham (Rhodophyceae) to sub-lethal copper concentrations. Aquat. Toxicol., 64: 201–213.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cotou E, Henry M, Zeri C et al. 2012. Short-term exposure of the European sea bass Dicentrarchus labrax to copperbased antifouling treated nets: copper bioavailability and biomarkers responses. Chemosphere, 89(9): 1 091–1 097.

    Article  Google Scholar 

  • Evans L V. 1981. Marine algae and fouling: a review, with particular reference to ship-fouling. Bot. Mar. 24: 167–171.

    Article  Google Scholar 

  • Fang R. 1991. Application of Atomic Absorption Spectroscopy in Sanitary Test. Beijing University Press, Beijing. p.148–158.

    Google Scholar 

  • Farias W R, Valente A P, Pereira M S et al. 2000. Structure and anticoagulant activity of sulfated galactans. J. Biol. Chem., 275: 29 299–29 307.

    Article  Google Scholar 

  • Giannopolitis C N, Ries S K. 1977. Superoxide dismutase occurrence in higher plants. Plant Physiol., 59: 304–314.

    Google Scholar 

  • Haglund K, Björklund M, Gunnare S et al. 1996. New method for toxicity assessment in marine and brackish environments using the macroalga Gracilaria tenuistipitata (Gracilariales, Rhodophyta). Hydrobiologia, 326: 317–325.

    Article  Google Scholar 

  • Han T J, Kang S H, Park J S et al. 2008. Physiological responses of Ulva pertusa and U. armoricana to copper exposure. Aquatic Toxicology, 86: 176–184.

    Article  Google Scholar 

  • Hashim M A, Chu K H. 2004. Biosorption of cadmium by brown, green, and red seaweeds. Chem. Eng. J., 97: 249–255.

    Article  Google Scholar 

  • Huo Y Z, Xu S N, Wang Y Y et al. 2011. Bioremediation efficiencies of Gracilaria verrucosa cultivated in an enclosed sea area of Hangzhou Bay, China. J. Appl. Phycol., 23:173–182.

    Article  Google Scholar 

  • Huo Y Z, Xu S N, Wang Y Y et al. 2012. Bioremediation efficiency of Gracilaria verrucosa for an integrated multitrophic aquaculture system with Pseudosciaena crocea in Xiangshan harbor, China. Aquaculture, 329: 99–105.

    Article  Google Scholar 

  • Jimenez A, Hernandez J A, del Rio L A et al. 1997. Evidence for the presence of ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol., 114: 275–284.

    Google Scholar 

  • Kaladharan P, Vijayakumaran K, Chennubhotla V S K. 1996. Optimization of certain physical parameters for the mariculture of Gracilaria edulis (Gmelin) Silva in Minicoy lagoon (Laccadive Archipelago). Aquaculture, 139: 265–270.

    Article  Google Scholar 

  • Küpper H, Šetlík I, Spiller M et al. 2002. Heavy metal induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J. Phycol., 38: 429–441.

    Google Scholar 

  • Kursar T A, van der Meer J P, Alberte R S. 1983. Lightharvesting system of the red alga Gracilaria tekvahiae. I. Biochemical analysis of pigment mutations. Plant Physiology, 73: 353–360.

    Article  Google Scholar 

  • Lei Y, Korpelainen H, Li C. 2007. Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere, 68: 686–694.

    Article  Google Scholar 

  • Lewis A G, Metaxas A. 1991. Concentrations of total dissolved copper in and near a copper-treated salmon net pen. Aquaculture, 99: 269–276.

    Article  Google Scholar 

  • Macfie S M, Welbourn P M. 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  Google Scholar 

  • Mal T K, Adorjan P, Gorbett A L. 2002. Effect of copper on growth of an aquatic macrophyte Elodea Canadensis. Environ. Pollut., 120: 307–311.

    Article  Google Scholar 

  • Martins C, Barcarolli I F, Menezes E J et al. 2011. Acute toxicity, accumulation and tissue distribution of copper in the blue crab Callinectes sapidus acclimated to different salinities: in vivo and in vitro studies. Aquatic Toxicology, 101(1): 88–99.

    Article  Google Scholar 

  • Maxwell K, Johnson G N. 2000. Chlorophyll fluorescence a practical guide. J. Exp. Bot., 51: 659–668.

    Article  Google Scholar 

  • Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant Cell Physiol., 22: 76–80.

    Google Scholar 

  • Prasad M N V, Malec P, Waloszek A et al. 2001. Physiological responses of Lemna trisulca L. (duckweed) to cadmium and copper bioaccumulation, Plant Sci., 161: 881–889.

    Article  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new modulation fluorometer. Photosynth. Res., 10: 51–62.

    Article  Google Scholar 

  • Sgherri C L M, Loggini B, Puliga S et al. 1994. Antioxidant defense system in Sporobolus stapfianus: changes in response to dessication and rehydration. Phytochemistry, 33: 561–565.

    Article  Google Scholar 

  • Stauber J L, Florence T M. 1987. Mechanism of toxicity of ionic copper and copper complexes to algae. Mar. Biol., 94: 511–519.

    Article  Google Scholar 

  • Stengel D B, Macken A, Morrison L et al. 2004. Zinc concentrations in marine macroalgae and lichen from western Ireland in relation to phylogenetic grouping, habitat and morphology. Mar. Poll. Bull., 48: 902–909.

    Article  Google Scholar 

  • Sudhakar C, Lakshmi A, Giridarakumar S. 2001. Changes in the antioxidant enzymes efficacy in two high yielding genotypes of mulberry (Morusalba L.) under NaCl salinity. Plant Sci., 161: 613–9.

    Article  Google Scholar 

  • Tang K X, Yuan D X, Lin S B et al. 2003. Depression and affect of red tide on main water quality index by Gracilaria tenuistipitata. Mar. Environ. Sci., 22: 24–27.

    Google Scholar 

  • Tanyolac D, Ekmekci Y, Ünalan S. 2007. Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere, 67: 89–98.

    Article  Google Scholar 

  • Van-Heerden P D R, Robertson B L, De-Kock L. 1997. Inhibition of Ectocarpus siliculosus infestations with copper chloride in tank cultures of Gracilaria gracilis. J. Appl. Phycol., 9: 255–259.

    Article  Google Scholar 

  • Virginia G R, Yolanda F P, Daniel R et al. 2007. Cell wall composition affects Cd2+ accumulation and intracellular thiol peptides in marine red algae. Aquatic Toxicology, 81: 65–72.

    Article  Google Scholar 

  • Wellburn A R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol., 144: 307–313.

    Article  Google Scholar 

  • Xu Y J, Fang J G, Wei W. 2008. Application of Gracilaria lichenoides (Rhodophyta) for alleviating excess nutrients in aquaculture. Journal of Applied Phycology, 20: 199–203.

    Article  Google Scholar 

  • Yang Y F, Fei X G, Song J M et al. 2006. Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture, 254: 248–255.

    Article  Google Scholar 

  • Yu J Q, Zhou Y H, Huang L F et al. 2002. Chill-induced inhibition of photosynthesis: genotypic variation within Cucumis sativus. Plant Cell Physiol., 43: 1 182–1 188.

    Article  Google Scholar 

  • Yun Y S, Park D, Park J M et al. 2001. Biosorption of trivalent chromium on the brown seaweed biomass. Environ. Sci. Technol., 35(21): 4 353–4 358.

    Article  Google Scholar 

  • Zhou Y, Yang H S, Hu H Y et al. 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

Author information

Authors and Affiliations

  1. College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, China

    Hezhong Huang  (黄鹤忠) & Jiansheng Liang  (梁建生)

  2. School of Basic Medicine and Biological Science, Soochow University, Suzhou, 215123, China

    Hezhong Huang  (黄鹤忠), Xiaosong Wu  (吴小松), Hao Zhang  (张皓), Qianqian Li  (李倩倩) & Qunying Zhang  (张群英)

Authors
  1. Hezhong Huang  (黄鹤忠)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiansheng Liang  (梁建生)
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaosong Wu  (吴小松)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hao Zhang  (张皓)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qianqian Li  (李倩倩)
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qunying Zhang  (张群英)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiansheng Liang  (梁建生).

Additional information

Supported by the Society Development Program of the Natural Science Foundation of Jiangsu Province in China (No. BS2002016)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, H., Liang, J., Wu, X. et al. Comparison in copper accumulation and physiological responses of Gracilaria lemaneiformis and G. lichenoides (Rhodophyceae). Chin. J. Ocean. Limnol. 31, 803–812 (2013). https://doi.org/10.1007/s00343-013-2261-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-013-2261-5

Keyword

Search

Navigation