Journal of Applied Phycology

, Volume 25, Issue 2, pp 369–378 | Cite as

The ameliorating effect of Acadian marine plant extract against ionic liquids-induced oxidative stress and DNA damage in marine macroalga Ulva lactuca

  • Manoj Kumar
  • C. R. K. ReddyEmail author
  • Bhavanath Jha


Ionic liquids (ILs) are generally considered as the green replacement for conventional volatile organic solvents. Nonetheless, their high solubility in water with proven toxic effects on aquatic biota has questioned their green credentials. In the present study, the detoxification potential of Acadian marine plant extract powder (AMPEP) prepared from the brown alga Ascophyllum nodosum was investigated against the 1-alkyl-3-methylimidazolium bromide [C12mim]Br ionic liquid-induced toxicity and oxidative stress in marine macroalga Ulva lactuca. The IL ([C12mim]Br) at LC50 (70 μM) exposure triggered the generation of reactive oxygen species (ROS) such as O 2 ·− , H2O2 and OH· causing membrane and DNA damage together with inhibition of antioxidant systems in the alga. The supplementation of AMPEP (150 μg mL−1) to the culture medium significantly reduced the accumulation of ROS and lipid peroxidation together with the inhibition of lipoxygenase (LOX) activity specially LOX-2 and LOX-3 isoforms. This is for the first time wherein comet assay was performed to ascertain the protective role of AMPEP against DNA damage in algal tissue grown in medium supplemented with IL and AMPEP. The AMPEP showed protective role against DNA damage (5–45 % tail DNA) when compared to those of grown in IL alone (45–70 % tail DNA). Further, specific isomorphs of different antioxidant enzymes such as superoxide dismutase (Mn-SOD-1, ~150 kDa), ascorbate peroxidase (APX-4, ~55 kDa), glutathione peroxidase (GSH-Px-2, ~55 kDa) and glutathione reductase (GR-1, ~180 kDa) responded specifically to AMPEP supplementation. It is evident from these findings that AMPEP could possibly be used for circumventing the negative effects arising from ILs-induced toxicity in marine ecosystem.


Ionic liquid AMPEP Marine algae DNA damage Ulva lactuca Ascophyllum nodosum 



The first author (MK) gratefully acknowledges the Council of Scientific and Industrial Research, New Delhi, India for Senior Research Fellowship. We are especially grateful to Dr Alan T. Critchley (Acadian Seaplants Limited, Canada) for generously providing the Acadian marine plant extract powder and offering valuable suggestions on the first draft of manuscript.


  1. APPA (2010) The Asian network for using algae as a CO2 sink. The Asia Pacific Phycological Association. News letter (6), 1 December 2010.Google Scholar
  2. Bernot RJ, Kennedy EE, Lamberti GA (2005) Effects of ionic liquids on the survival, movement, and feeding behavior of the freshwater snail, Physa acuta. Environ Toxicol Chem 24:1759–1765PubMedCrossRefGoogle Scholar
  3. Bonhote P, Dias AP, Papageorgiou N, Kalyanasundaram K, Gratzel M (1996) Hydrophobic, highly conductive ambient temperature molten salts. Ing Chem 35:1168–1178Google Scholar
  4. Cho CW, Jeon YC, Pham TPT, Vijayaraghavan K, Yun YS (2008) The ecotoxicity of ionic liquids and traditional organic solvents on microalga Selenastrum capricornutum. Ecotoxicol Environ Safe 71:166–171CrossRefGoogle Scholar
  5. Coleman D, Gathergood N (2010) Biodegradation studies of ionic liquids. Chem Soc Rev 39:600–637PubMedCrossRefGoogle Scholar
  6. Couling DJ, Bernot RJ, Docherty KM, Dixon JK, Maginn EJ (2006) Assessing the factors responsible for ionic liquid toxicity to aquatic organisms via quantitative structure-property relationship modelling. Green Chem 8:82–90CrossRefGoogle Scholar
  7. Earle MJ, Seddon KR (2000) Ionic liquids: green solvents for the future. Pure Appl Chem 72:1391–1398CrossRefGoogle Scholar
  8. Fan D, Hodges DM, Zhang J, Kirby CW, Ji X, Locke SJ, Critchley AT, Prithiviraj B (2011) Commercial extract of the brown seaweed Ascophyllum nodosum enhances phenolic antioxidant content of spinach (Spinacia oleracea L.) which protects Caenorhabditis elegans against oxidative and thermal stress. Food Chem 124:195–202CrossRefGoogle Scholar
  9. Garcia O, Romerob I, Gonzalez J, Mandina ET (2007) Measurements of DNA damage on silver stained comets using free Internet software. Mutat Res 627:186–190PubMedCrossRefGoogle Scholar
  10. Hazra B, Biswas S, Mandal N (2008) Antioxidant and free radical scavenging activity of Spondias pinnata. BMC Complement Altern Med 8:63–72PubMedCrossRefGoogle Scholar
  11. Holdt SL, Kraan S (2010) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  12. Hurtado AQ, Yunque DA, Tibubos K, Critchley AT (2009) Uses of Acadian marine plant extract powder from Ascophyllum nodosum in tissue culture of Kappaphycus varieties. J Appl Phycol 21:633–639CrossRefGoogle Scholar
  13. Jayaraj J, Norrie J, Punja ZK (2011) Commercial extract from the brown seaweed Ascophyllum nodosum reduces fungal diseases in greenhouse cucumber. J Appl Phycol 23:353–361CrossRefGoogle Scholar
  14. Khan W, Palanisamy R, Hankins SD, Critchley AT, Smith DL, Papadopoulos Y, Prithiviraj B (2008) Ascophyllum nodosum (L.) Le Jolis extract improves root nodulation in alfalfa. Can J Plant Sci 88:728–728Google Scholar
  15. Khan W, Hiltz D, Critchley AT, Prithiviraj B (2010) Bioassay to detect Ascophyllum nodosum extract-induced cytokinin-like activity in Arabidopsis thaliana. J Appl Phycol 23:409–414CrossRefGoogle Scholar
  16. Kumar M, Kumari P, Gupta V, Anisha PA, Reddy CRK, Jha B (2010a) Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta). Biometals 23:315–325PubMedCrossRefGoogle Scholar
  17. Kumar M, Kumari P, Gupta V, Reddy CRK, Jha B (2010b) Biochemical responses of red alga Gracilaria corticata (Gracilariales, Rhodophyta) to salinity induced oxidative stress. J Exp Mar Biol Ecol 391:27–34CrossRefGoogle Scholar
  18. Kumar M, Trivedi N, Reddy CRK, Jha B (2011a) Toxic effects of imidazolium ionic liquids on the green seaweeds Ulva lactuca: oxidative stress and DNA damage. Chem Res Toxicol 24:1882–1890PubMedCrossRefGoogle Scholar
  19. Kumar M, Gupta V, Trivedi N, Kumari P, Bijo AJ, Reddy CRK, Jha B (2011b) Desiccation induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ Exp Bot 72:194–201CrossRefGoogle Scholar
  20. Kumar M, Bijo AJ, Baghel RS, Reddy CRK, Jha B (2012) Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiol Biochem 51:129–138PubMedCrossRefGoogle Scholar
  21. Latala A, Nedzi M, Stepnowski P (2010) Toxicity of imidazolium ionic liquids towards algae: Influence of salinity variations. Green Chem 12:60–64CrossRefGoogle Scholar
  22. Liu Y, Jiang H, Zhao Z, An L (2010) Nitric oxide synthase like activity-dependent nitric oxide production protects against chilling-induced oxidative damage in Chorispora bungeana suspension cultured cells. Plant Physiol Biochem 48:936–944PubMedCrossRefGoogle Scholar
  23. Loureiro RR, Reis RP, Berrogain FD, Critchley AT (2011) Extract powder from the brown alga Ascophyllum nodosum (Linnaeus) Le Jolis (AMPEP): a “vaccine-like” effect on Kappaphycus alvarezii (Doty) Doty ex P.C. Silva. J Appl Phycol doi 10.1007/s10811-011-9735-7.
  24. Nadin SB, Vargas-Roig LM, Ciocca DR (2011) A silver staining method for single-cell gel assay. J Histochem Cytochem 49:1183–1186CrossRefGoogle Scholar
  25. Pham TPT, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: a review. Water Res 44:352–357PubMedCrossRefGoogle Scholar
  26. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collection of algae. Japanese Society of Plant Physiologists, Tokyo, pp 63–67Google Scholar
  27. Queguineur B, Kraan S, Guiry MD, Ramos S, Martin MA, Goya L, Mateos R, Bravo L (2012) Effect of phlorotannin-rich extracts of Ascophyllum nodosum and Himanthalia elongata (Phaeophyceae) on cellular oxidative markers in human HepG2 cells. J Appl Phycol. doi: 10.1007/s10811-012-9832-2
  28. Ranke J, Müller A, Bottin-Weber U, Stock F, Stolte S, Arning J, Störmann R, Jastorff B (2007) Lipophilicity parameters for ionic liquid cations and their correlation to in vitro cytotoxicity. Ecotoxicol Environ Safe 67:430–438CrossRefGoogle Scholar
  29. Romero A, Santos A, Tojo J, Rodriguesz A (2008) Toxicity and biodegradability of imidazolium ionic liquids. J Hazard Mater 151:268–273PubMedCrossRefGoogle Scholar
  30. Shiu CT, Lee TM (2005) Ultraviolet-B induced oxidative stress and response of the ascorbate glutathione cycle in a marine macroalga Ulva fasciata. J Exp Bot 56:2851–2865PubMedCrossRefGoogle Scholar
  31. Willekens HD, Inze M, Montagu MV, Camp WV (1995) Catalase in plants. Mol Breeding 1:207–228CrossRefGoogle Scholar
  32. Yu M, Wang SH, Luo YR, Han YW, Li XY, Zhang BJ, Wang JJ (2009) Effects of 1-alkyl-3-methylimidazolium bromide ionic liquids on the antioxidant defence system of Daphnia magna. Ecotoxicol Environ Safe 72:1798–1804CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Discipline of Marine Biotechnology and EcologyCSIR-Central Salt and Marine Chemicals Research InstituteBhavnagarIndia

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