Oxidative Stress and Antioxidant Activities of Intertidal Macroalgae in Korea

  • Park, Jung-Jin (Department of Chemistry, University of Incheon) ;
  • Han, Tae-Jun (Division of Life Sciences, University of Incheon) ;
  • Choi, Eun-Mi (Department of Chemistry, University of Incheon)
  • Received : 2011.10.18
  • Accepted : 2011.12.05
  • Published : 2011.12.31


The oxidative stress level and antioxidant activities in two green algae (Ulva pertusa and Ulva linza), two brown algae (Agarum cribrosum and Dictyota dichotoma), and three red algae (Grateloupia lanceolata, Carpopeltis affinis, and Gracilaria verrucosa) collected from intertidal regions of Korea were assessed. In the two green algae, although the total glutathione content was not as high as that of the brown algae, the glutathione pool was extremely reduced, and the glutathione reductase (GRd)/glutathione peroxidase (GPx) activity ratio was high, which apparently plays an important role for protection against oxidative damage, as manifested by low lipid peroxidation. In the brown algae, which exhibited a low lipid peroxidation level that was comparable to the green algal species, the highest glutathione content, together with high GPx activity, appears to be the most important factor in their antioxidant protection. The red algal species exhibited extremely high lipid peroxidation levels. They also contained the lowest and most oxidized glutathione among the species, as well as the lowest GRd activity. In spite of the marked difference in the glutathione content, the significant difference in the activity of ${\gamma}$-glutamylcysteine ligase, the rate limiting enzyme for glutathione synthesis, among the species was not exhibited. Our results suggest that there is a significant difference in the levels of oxidative stress and antioxidant capacity among the algal species, and that the glutathione system, especially the efficiency of glutathione recycling, plays a vital role in antioxidative protection in algal species.


Supported by : University of Incheon


  1. Fleurence J. 1999. Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Tech 10: 25-28.
  2. Kuda T, Goto H, Yokoyama M, Fujii T. 1998. Fermentation of dietary fiber in dried products of brown algae and their effects on fecal microflora and levels of plasma lipid in rats. Fisheries Sci 64: 582-588.
  3. Berge JP, Debiton E, Dumay J, Durand P, Barthomeuf C. 2002. In vitro anti-inflammatory and anti-proliferative activity of sulfolipids from the red alga Porphyridium cruentum. J Agric Food Chem 50: 6227-6232.
  4. Ellouali M, Boisson-Vidal C, Durand P, Jozefonvicz J. 1993. Antitumor activity of low molecular weight fucans extracted from brown seaweed Ascophyllum nodosum. Anticancer Res 13: 2011-2020.
  5. De la Coba F, Aguilera J, Figueroa FL, de Gálvez MV, Herrera E. 2009. Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J Appl Phycol 21: 161-169.
  6. Wang J, Zhang Q, Zhang Z, Li Z. 2008. Antioxidant activity of sulfated polysaccharide fractions extracted from Laminaria japonica. Int J Biol Macromols 42: 127-132.
  7. Yuan YV, Walsh NA. 2006. Antioxidant and antiproliferative activities of extracts from a variety of edible seaweeds. Food Chem Toxicol 44: 1144-1150.
  8. Foyer CH, Noctor G. 2003. Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146: 359-388.
  9. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN. 2006. Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141: 357-366.
  10. Dring MJ. 2006. Stress resistance and disease resistance in see weeds: the role of reactive oxygen metabolism. Adv Bot Res 43: 175-207.
  11. Han T, Kang SH, Park JS, Lee HK, Brown MT. 2008. Physiological responses of Ulva pertusa and U. armoricana to copper exposure. Aqua Toxicol 86: 176-184.
  12. Lesser MP. 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68: 253-278.
  13. De Gara L, de Pintoa MC, Tommasia F. 2003. The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41: 863-870.
  14. Selvakumar V. 2008. Ultraviolet-B radiation (280-315 nm) invoked antioxidant defence systems in Vigna unguiculata (L.) Walp. and Crotalaria juncea L. Photosynthetica 46: 98-106.
  15. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic- Jovanovic S, Verrier PJ, Noctor G, Foyer CH. 2003. Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15: 939-951.
  16. Wojtaszek P. 1997. Oxidative burst: an early plant response to pathogen infection. Biochem J 322: 681-692.
  17. Choo KS, Pedersen M, Snoeojis P. 2004. Oxidative stress tolerence in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana. J Exp Mar Biol Ecol 298: 111-123.
  18. Slesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z. 2007. The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. Acta Biochim Pol 54: 39-50.
  19. Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358.
  20. Reed DJ, Babson JR, Beatty PW, Brodie AE, Ellis WW, Potter DW. 1980. High-performance liquid chromatography analysis of nanomole levels of glutathione, glutathione disulfide, and related thiols and disulfides. Anal Biochem 106: 55-62.
  21. Seelig GF, Meister A. 1984. Gamma-glutamylcysteine synthetase from erythrocytes. Anal Biochem 141: 510-514.
  22. Paglia DE, Valentine WN. 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70: 158-169.
  23. Cohen MB, Duvel DL. 1988. Characterization of the inhibition of glutathione reductase and the recovery of enzyme activity in exponentially growing murine leukemia (L1210) cells treated with 1,3-bis(2-chloroethyl)-1-nitrosourea. Biochem Pharmacol 37: 3317-3320.
  24. McCord JM, Fridovich I. 1969. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244: 6049-6055.
  25. Aebi H. 1984. Catalase in vitro. Methods Enzymol 105: 121-126.
  26. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
  27. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
  28. Jensen A. 1993. Present and future needs for algae and algal products. Hydrobiol 260/261: 15-21.
  29. McDermid KJ, Stuercke B. 2003. Nutritional composition of edible Hawaiian seaweeds. J Appl Phycol 15: 513-524.
  30. Montgomery WL, Gerking SD. 1980. Marine macroalgae as foods for fishes: an evaluation of potential food quality. Env Biol Fish 5: 143-153.
  31. Kumar N, Kumar RN, Amb MK, Bora A, Chakraborty S. 2010. Variation of biochemical composition of eighteen marine macroalgae collected from Okha coast, Gulf of Kutch, India. EJEAFChe 9: 404-410.
  32. Ishikawa T, Shigeoka S. 2008. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72: 1143-1154.
  33. Eaton P, Byers HL, Leeds N, Ward MA, Shattock MJ. 2002. Detection, quantitation, purification, and identification of cardiac proteins S-thiolated during ischemia and reperfusion. J Biol Chem 277: 9806-9811.
  34. Thomas JA, Chai YC, Jung CH. 1994. Protein S-thiolation and dethiolation. Methods Enzymol 233: 385-395.
  35. Lauterburg BH, Smith CV, Hughes H, Mitchell JR. 1984. Biliary excretion of glutathione and glutathione disulfide in the rat. Regulation and response to oxidative stress. J Clin Invest 73: 124-133.
  36. O'Donovan DJ, Katkin JP, Tamura T, Husser R, Xu X, Smith CV, Welty SE. 1999. Gene transfer of mitochondrially targeted glutathione reductase protects H441 cells from t-butyl hydroperoxide-induced oxidant stresses. Am J Respir Cell Mol Biol 20: 256-263.
  37. Baier M, Dietz KJ. 2005. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 56: 1449-1462.
  38. Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM. 2004. Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16: 2448-2462.
  39. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R. 2005. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268-281.
  40. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inze D, Van Breusegem F. 2004. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39: 45-58.
  41. Lobban CS, Harrison PJ. 1997. Seaweed ecology and physiology. Cambridge University Press, New York, NY, USA. p 129.
  42. Park PJ, Kim EK, Lee SJ, Park SY, Kang DS, Jung BM, Kim KS, Je JY, Ahn CB. 2009. Protective effects against $H_2O_2$-induced damage by enzymatic hydrolysates of an edible brown seaweed, sea tangle (Laminaria japonica). J Med Food 12: 159-166.