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Physiological responses of Porphyra haitanensis (Rhodophyta) to copper and cadmium exposure

  • Xifeng Zhu

    Xifeng Zhu is Assistant Professor of Fisheries at the Institute of Animal Science, Guangdong Academy of Agricultural Science. He was awarded an MS in Marine Biology by Shantou University. More recent research has concentrated on algal physiology and animal nutrition and feed science.

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    , Dinghui Zou

    Dinghui Zou is Professor of Marine Biology at the College of Environment and Energy, South China University of Technology. He was awarded a PhD in Hydrobiology by the Institute of Hydrobiology, Chinese Academy of Sciences. More recent research has concentrated on algal physiology and applied phycology.

    , Yanhua Huang

    Yanhua Huang is Professor of Animal Nutrition and Feed Science at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded a PhD in Animal Nutrition and Feed Science by South China Agricultural University. More recent research has concentrated on animal nutrition and feed science.

    , Junming Cao

    Junming Cao is Professor of Animal Nutrition and Feed Science at the Institute of Animal Science, Guangdong Academy of Agricultural Science. He was awarded a PhD in Nutritional Physiology and Biochemistry by the University of Burgundy. More recent research has concentrated on animal nutrition and feed science.

    , Yuping Sun

    Yuping Sun is Associate Professor of Animal Nutrition and Feed Science at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded a PhD in Hydrobiology by Jinan University. More recent research has concentrated on animal nutrition and aquaculture.

    , Bing Chen

    Bing Chen is Associate Professor of Fisheries at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded an MS in Aquaculture by South China Agricultural University. More recent research has concentrated on animal nutrition and aquaculture.

    and Xiaoying Chen

    Xiaoying Chen is Assistant Professor of Fisheries at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded an MS in Aquaculture by South China Agricultural University. More recent research has concentrated on animal nutrition and aquaculture.

Published/Copyright: February 7, 2017

Abstract

The aim of the present work was to evaluate the effects of copper (Cu) and cadmium (Cd) on the physiology of the red macroalga Porphyra haitanensis Chang and Zheng. The alga was cultured in media with different Cu or Cd concentrations for 7 days. The relative growth rate was significantly reduced at Cu concentrations of 0.10 mg l−1 and above or at Cd concentrations of 4 mg l−1 and above. Chlorophyll a (Chl a), carotenoids (Car), phycoerythrin (PE) and phycocyanin (PC) contents decreased at high Cu or Cd concentrations, and PE content increased at 0.10 mg l−1 Cu or 4–8 mg l−1 Cd. Moreover, the optimal quantum yield, maximum net photosynthetic rate (Pm) and apparent photosynthetic efficiency (α) were significantly reduced at high Cu or Cd concentrations. In contrast, malondialdehyde (MDA) content and superoxide dismutase (SOD) activity increased in response to Cu or Cd treatment. Catalase activity increased at 2–8 mg l−1 Cd and significantly declined at 0.50 mg l−1 Cu or 10 mg l−1 Cd. Nitrate reductase (NR) activity declined at high Cu or Cd concentrations. Consequently, both Cu and Cd were physiological stressors for P. haitanensis, with Cu being more toxic than Cd. This work has generated valuable knowledge about the toxic effects of Cu and Cd on macroalgae.

About the authors

Xifeng Zhu

Xifeng Zhu is Assistant Professor of Fisheries at the Institute of Animal Science, Guangdong Academy of Agricultural Science. He was awarded an MS in Marine Biology by Shantou University. More recent research has concentrated on algal physiology and animal nutrition and feed science.

Dinghui Zou

Dinghui Zou is Professor of Marine Biology at the College of Environment and Energy, South China University of Technology. He was awarded a PhD in Hydrobiology by the Institute of Hydrobiology, Chinese Academy of Sciences. More recent research has concentrated on algal physiology and applied phycology.

Yanhua Huang

Yanhua Huang is Professor of Animal Nutrition and Feed Science at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded a PhD in Animal Nutrition and Feed Science by South China Agricultural University. More recent research has concentrated on animal nutrition and feed science.

Junming Cao

Junming Cao is Professor of Animal Nutrition and Feed Science at the Institute of Animal Science, Guangdong Academy of Agricultural Science. He was awarded a PhD in Nutritional Physiology and Biochemistry by the University of Burgundy. More recent research has concentrated on animal nutrition and feed science.

Yuping Sun

Yuping Sun is Associate Professor of Animal Nutrition and Feed Science at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded a PhD in Hydrobiology by Jinan University. More recent research has concentrated on animal nutrition and aquaculture.

Bing Chen

Bing Chen is Associate Professor of Fisheries at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded an MS in Aquaculture by South China Agricultural University. More recent research has concentrated on animal nutrition and aquaculture.

Xiaoying Chen

Xiaoying Chen is Assistant Professor of Fisheries at the Institute of Animal Science, Guangdong Academy of Agricultural Science. She was awarded an MS in Aquaculture by South China Agricultural University. More recent research has concentrated on animal nutrition and aquaculture.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (no. 41276148) and Science and Technology Planning Project of Guangdong (no. 2015 A020216004).

References

Abdallah, M.A.M. and A.M.A. Abdallah. 2008. Biomonitoring study of heavy metals in biota and sediments in the South Eastern coast of Mediterranean sea, Egypt. Environ. Monit. Assess. 146: 139–145.10.1007/s10661-007-0066-8Search in Google Scholar

Aebi, H. 1984. Catalase in vitro. In: (L. Packer, ed.) Methods in enzymology. Volume 105. Academic Press Inc., San Diego, CA. pp. 121–126.10.1016/S0076-6879(84)05016-3Search in Google Scholar

Aggarwal, A., I. Sharma, B.N. Tripathi, A.K. Munjal, M. Baunthiyal and V. Sharma. 2011. Metal toxicity and photosynthesis. In: (S. Itoh, P. Mohanty and K.N. Guruprasad, eds.) Photosynthesis: Overviews on RecentProgress & Future Perspective. IK International Publishing House, New Delhi. pp. 229–236.Search in Google Scholar

Babu, M.Y., L. Palanikumar, N. Nagarani, V.J. Devi, S.R. Kumar, C.M. Ramakritinan and A.K. Kumaraguru. 2014. Cadmium and copper toxicity in three marine macroalgae: evaluation of the biochemical responses and DNA damage. Environ. Sci. Pollut. Res. 21: 9604–9616.10.1007/s11356-014-2999-0Search in Google Scholar

Baumann, H.A., L. Morrison and D.B. Stengel. 2009. Metal accumulation and toxicity measured by PAM–Chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol. Environ. Saf. 72: 1063–1075.10.1016/j.ecoenv.2008.10.010Search in Google Scholar

Beauchamp, C. and I. Fridovich. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44: 276–287.10.1016/0003-2697(71)90370-8Search in Google Scholar

Beer S. and A. Eshel. 1985. Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Aust. J. Mar. Freshw. Res., 36: 785–792.10.1071/MF9850785Search in Google Scholar

Berges, D. 1997. Algal nitrate reductase. Eur.J. Phycol. 32: 3–8.10.1080/09541449710001719315Search in Google Scholar

Bertrand, M. and I. Poirier. 2005. Photosynthetic organisms and excess of metals. Photosynthetica. 43: 345–353.10.1007/s11099-005-0058-2Search in Google Scholar

Bradford, M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.10.1016/0003-2697(76)90527-3Search in Google Scholar

Brown, M.T. and J.E. Newman. 2003. Physiological responses of Gracilariopsis longissima (S.G.Gmelin) Steentoft, L.M. Irvine and Farnham (Rhodophyceae) to sub-lethal copper concentrations. Aquat. Toxicol.64: 201–213.10.1016/S0166-445X(03)00054-7Search in Google Scholar

Cakmak, I. 2000. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 146: 185–205.10.1046/j.1469-8137.2000.00630.xSearch in Google Scholar PubMed

Chow, F., M.C. de Oliveira and M. Pedersén. 2004. In vitro assay and light regulation of nitrate reductase in red alga Gracilaria chilensis. J. PlantPhysiol. 161: 769–776.10.1016/j.jplph.2004.01.002Search in Google Scholar

Cohen, G., M. Kim and V. Ogwu. 1996. A modified catalase assay suitable for a plate reader and for the analysis of brain cell cultures. J. Neurosci. Met. 67: 53–56.10.1016/0165-0270(96)00011-8Search in Google Scholar

Collén, J., E. Pioto, M. Pedersén and P. Colepicolo. 2003. Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Arch. Environ. Contam. Toxicol. 45: 337–342.10.1007/s00244-003-0196-0Search in Google Scholar

Corzo, A. and F.X. Niell. 1991. Determination of nitrate reductase activity in Ulva rigida C. Agardh by the in situ method. J. Exp. Mar. Biol. Ecol. 146: 181–191.10.1016/0022-0981(91)90024-QSearch in Google Scholar

Fernandez-Leborans, G. and A. Novillo. 1996. Toxicity and bioaccumulation of cadmium in Olisthodiscus luteus (Raphidophyceae). Water Res. 30: 57–62.10.1016/0043-1354(95)00084-XSearch in Google Scholar

Gaete Olivares, H., N. Moyano Lagos, C. Jara Gutierrez, R. Carrasco Kittelsen, G. Lobos Valenzuela and M.E. Hidalgo Lillo. 2016. Assessment oxidative stress biomarkers and metal bioaccumulation in macroalgae from coastal areas with mining activities in Chile. Environ. Monit. Assess. 188: 25.10.1007/s10661-015-5021-5Search in Google Scholar

Gledhill, M., M. Nimmo, S.J. Hill and M.T. Brown. 1997. The toxicity of copper (II) species to marine algae, with particular reference to macroalgae. J. Phycol. 33: 2–11.10.1111/j.0022-3646.1997.00002.xSearch in Google Scholar

Greger, M. and E. Ögren. 1991. Direct and indirect effects of Cd2+ on photosynthesis in sugar beet (Beta vulgaris). Physiol. Plant. 83: 129–135.10.1111/j.1399-3054.1991.tb01291.xSearch in Google Scholar

Halliwell, B. and J.M.C. Gutteridge. 1999. Free radicals in biology and medicine, third edition. Oxford University Press, Oxford.Search in Google Scholar

Han, H., S.-H. Kang, J.-S. Park, H.-K. Lee and M. T. Brown. 2008. Physiological responses of Ulva pertusa and Ulva armoricana to copper exposure. Aquat. Toxicol. 86: 176–184.10.1016/j.aquatox.2007.10.016Search in Google Scholar

Health, R.L. and L. Packer. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125: 189–198.10.1016/0003-9861(68)90654-1Search in Google Scholar

Henley, W.J. 1993. Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J. Phycol. 29: 729–739.10.1111/j.0022-3646.1993.00729.xSearch in Google Scholar

Huang, X., C. Ke and W.-X. Wang. 2010. Cadmium and copper accumulation and toxicity in the macroalga Gracilaria tenuistipitata. Aquat. Biol. 11:17–26.10.3354/ab00288Search in Google Scholar

Hurd C.L., P.J. Harrison, K. Bischof and C.S. Lobban. 2014. Seaweed ecology and physiology. Cambridge University Press, Cambridge.10.1017/CBO9781139192637Search in Google Scholar

Jiang, H., K. Gao and E.W. Helbling. 2009. The conchocelis of Porphyra haitanensis (Rhodophyta) is protected from harmful UV radiation by the covering calcareous matrix. J. Phycol. 45: 1270–1277.10.1111/j.1529-8817.2009.00755.xSearch in Google Scholar PubMed

Küpper, H., F.C. Küpper and M. Spiller. 1996. Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J. Exp. Bot. 47: 259–266.10.1093/jxb/47.2.259Search in Google Scholar

Li Y.X., S. Zhou, F.J. Zhao, Y. Liu, P.P. Fan and G.C. Wang. 2010. Physiological responses of Porphyra haitanesis to different copper and zinc concentrations. Braz. J. Oceanogr. 58: 261–267.10.1590/S1679-87592010000400001Search in Google Scholar

Maxwell, K. and G.N. Johnson. 2000. Chlorophyll fluorescence–a practical guide. J. Exp. Bot. 51: 659–668.10.1093/jexbot/51.345.659Search in Google Scholar

Millward, G.E. and A. Turner. 2001. Metal pollution. In: (J.H. Steele, S.A. Thorpe and S.A. Turekian, eds.) Encyclopedia of ocean sciences. Academic Press, San Diego, CA. pp. 1730–1737.10.1006/rwos.2001.0054Search in Google Scholar

Okamoto, O.K., E. Pinto, L.R. Latorre, E.J.H. Bechara and P. Colepicolo. 2001. Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch. Environ. Contam. Toxicol. 40: 18–24.10.1007/s002440010144Search in Google Scholar PubMed

Pätsikkä, E., E.-M. Aro and E. Tyystjärvi. 2001. Mechanism of copper-enhanced photoinhibition in thylakoid membranes. Physiol. Plant. 113: 142–150.10.1034/j.1399-3054.2001.1130119.xSearch in Google Scholar

Ramus, J. 1992. Productivity of seaweeds. In: (P.G. Falkowski and A.D. Woodhead, eds.) Primary productivity and biogeochemical cycles in the sea. Plenum Press, New York. pp. 239–255.10.1007/978-1-4899-0762-2_13Search in Google Scholar

Sandamann, G. and P. Böer. 1980. Copper-mediated lipid peroxidation processes in the photosynthetic membranes. PlantPhysiol. 66: 797–800.10.1104/pp.66.5.797Search in Google Scholar

Siedlecka, A. and Z. Krupa. 1996. Interaction between cadmium and iron and its effects on photosynthetic capacity of primary leaves of Phaseolus vulgaris.Plant Physiol. Biochem. 35: 951–957.Search in Google Scholar

Stauber, J.L. and T.M. Florence. 1987. Mechanism of toxicity of ionic copper and copper complexes to algae. Mar. Biol. 94: 511–519.10.1007/BF00431397Search in Google Scholar

Tang, X. and X. Fei. 1997. The relationship between light, temperature and growth, development of free-living conchocelis of Porphyra haitanensis. Oceanol. Limnol. Sin. 28: 475–482.Search in Google Scholar

Torres, M., M. Barros, S. Campos, E., Pinto, S. Rajamani, R. Sayre and P. Colepicolo. 2008. Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol. Environ. Saf.71: 1–15.10.1016/j.ecoenv.2008.05.009Search in 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. Plant Physiol. 144: 307–313.10.1016/S0176-1617(11)81192-2Search in Google Scholar

Xia, J.R., Y.Y. Li, J. Lu and B. Chen. 2004. Effects of copper and cadmium on growth, photosynthesis, and pigment content in Gracilaria lemaneiformis. Bull. Environ. Contam. Toxicol. 73: 979–986.10.1007/s00128-004-0522-xSearch in Google Scholar PubMed

Yang, Y. F., X.G. Fei, J.M. Song, H.Y. Hu, G.C. Wang and I.K. Chung. 2006. Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture. 254: 248–255.10.1016/j.aquaculture.2005.08.029Search in Google Scholar

Young, E.B., P.S. Lavery, B. van Elven, M.J. Dring and J.A. Berges. 2005. Nitrate reductase activity in macroalgae and its vertical distribution in macroalgal epiphytes of seagrasses. Mar. Ecol. Prog. Ser. 288: 103–114.10.3354/meps288103Search in Google Scholar

Zhu, X., D. Zou and H. Du. 2011. Physiological responses of Hizikia fusiformis (Phaeophyta) to copper and cadmium exposure. Bot. Mar. 54: 431–439.10.1515/BOT.2011.054Search in Google Scholar

Zhu, X., D. Zou, Y. Huang, J. Cao, G. Sheng and G. Wang. 2015. Physiological responses of Hizikia fusiformis (Phaeophyta) to mercury exposure. Bot. Mar. 58: 93–101.10.1515/bot-2014-0068Search in Google Scholar

Zou, D. 2005. Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiformis (Sargassaceae, Phaeophyta). Aquaculture250: 726–735.10.1016/j.aquaculture.2005.05.014Search in Google Scholar

Zou, D. and K. Gao. 2002. Effects of desiccation and CO2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China. Eur. J. Phycol. 37: 587–592.10.1017/S0967026202003876Search in Google Scholar

Received: 2016-10-27
Accepted: 2016-12-22
Published Online: 2017-2-7
Published in Print: 2017-2-1

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