Physiological responses of Cladophora glomerata to cyanotoxins: a potential new phytoremediation species for the Green Liver Systems

Toxicological and Environmental Chemistry

Volumn 98, Issue 2, 2016, Pages 241-259

  Pflugmacher, Stephan ^a,b   Kwon, Kyu Sang ^b   Baik, Seungyun ^c   Kim, Sanghum ^c   Kühn, Sandra ^a   Esterhuizen Londt, Maranda ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b Korea Institute of Science and Technology   (South Korea)

^c Korea Institute of Science and Technology Europe (KIST Europe)   (Germany)

Author keywords

algae; biotransformation; cyanotoxins; Green Liver System; oxidative stress response

Indexed keywords

ALGAE; BIOCHEMISTRY; BIOREMEDIATION; EUTROPHICATION; PHYSIOLOGICAL MODELS; POLLUTION; POTABLE WATER; PURIFICATION; TOXIC MATERIALS; WATER CONSERVATION; WATER TREATMENT PLANTS;

ANTI-OXIDATIVE STRESS; BIOTRANSFORMATION; CERATOPHYLLUM DEMERSUM; CYANOTOXINS; GREEN LIVER SYSTEM; OXIDATIVE STRESS RESPONSE; PHYSIOLOGICAL RESPONSE; TOXIN INTERNALIZATION;

WATER POLLUTION;

ANTHROPOGENIC SOURCE; AQUATIC PLANT; BIOLOGICAL UPTAKE; BIOTRANSFORMATION; CYANOBACTERIUM; EUTROPHICATION; GREEN ALGA; PHYSIOLOGICAL RESPONSE; PHYTOREMEDIATION; PURIFICATION; TOXIN; WATER POLLUTION; WATER TREATMENT; XENOBIOTICS;

ALGAE; CERATOPHYLLUM DEMERSUM; CLADOPHORA GLOMERATA; MYRIOPHYLLUM SPICATUM;

EID: 84955168844     PISSN: 02772248     EISSN: 10290486     Source Type: Journal    
DOI: 10.1080/02772248.2015.1119835     Document Type: Article

References (62)

1. P.Aravind,, and M.N.V.Prasad. 2005. “Modulation of Cadmium-Induced Oxidative Stress in Ceratophyllum Demersum by Zinc Involves Ascorbate-Glutathione Cycle and Glutathione Metabolism.” Plant Physiology and Biochemistry 43: 107–116. doi:10.1016/j.plaphy.2005.01.002.
2. A.Ballot,, L.Krienitz, K.Kotut, C.Wiegand, J.Metcalf, G.A.Codd, and S.Pflugmacher. 2004. “Cyanobacteria and Cyanobacterial Toxins in Three Alkaline Rift Valley Lakes of Kenya–Lakes Bogoria, Nakuru and Elmenteita.” Journal of Plankton Research 26: 925–935. doi:10.1093/plankt/fbh084.
3. D.J.Barrington,, A.Ghadouani, and G.N.Ivey. 2013. “Cyanobacterial and Microcystins Dynamic Following the Application of Hydrogen Peroxide to Waste Stabilisation Ponds.” Hydrological Earth System and Science 17: 2097–2105. doi:10.5194/hess-17-2097-2013.
4. M.M.Bradford, 1976. “Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing Principle of Protein-Dye Binding.” Analytical Biochemistry 72: 248–254. doi:10.1016/0003-2697(76)90527-3.
5. D.J.Cao,, X.D.Shi, H.Li, P.P.Xie, H.M.Zhang, J.W.Deng, and Y.G.Liang. 2014. “Effects of Lead on Tolerance, Bioaccumulation and Antioxidative Defense System of The Green Algae Cladophora.” Ecotoxicology and Environmental Safety 112: 231–237. doi:10.1016/j.ecoenv.2014.11.007.
6. I.Carlberg,, and B.Mannervik. 1985. “Glutathione Reductase Assay.” Methods in Enzymology 113: 484–495.
7. W.W.Carmichael, 1992. “Cyanobacteria Secondary Metabolites—The Cyanotoxins.” Journal of Applied Bacteriology 72 (6): 445–459.doi:10.1111/j.1365-2672.1992.tb01858.x.
8. W.Carmichael, 2008. “A World Overview—One-Hundred-Twenty-Seven Years of Research on Toxic Cyanobacteria—Where do We go from Here?” Advances in Experimental Medicine and Biology 619: 105–125.
9. S.J.Casper,, and H.D.Krausch. 1981. “Pteridophyta und Anthophyta, 2 Teil: Saururaceae bis Asteraceae.” Süsswasserflora von Mitteleuropa, Bd. 24: 413–943.
10. K.S.Choo,, P.Snoeijs, and M.Pedersen. 2004. “Oxidative Stress Tolerance in the Filamentous Green Algae Cladophora Glomerata and Enteromorpha Ahlneriana.” Journal of Experimental Marine Biology and Ecology 298: 111–123. doi:10.1016/j.jembe.2003.08.007.
11. A.Claiborne, 1985. “Catalase Activity.” In CRC Handbook of Methods for Oxygen Radical Research, edited by R.A.Greenwald, Boca Raton: CRC Press.
12. G.A.Codd, 2000. “Cyanobacterial Toxins, The Perception of Water Quality, and The Prioritisation of Eutrophication Control.” Ecological Engineering 16 (1): 51–60. doi:10.1016/S0041-0101(98)00244-X.
13. G.A.Codd,, J.S.Metcalf, and K.A.Beattie. 1999. “Retention of Microcystis Aeruginosa and Microcystin by Salad Lettuce (Lactuca Sativa) after Spray Irrigation with Water Containing Cyanobacteria.” Toxicon 37 (8): 1181–1185.
14. V.Contardo-Jara,, S.Kuehn, and S.Pflugmacher. 2015. “Single and Combined Exposure to MC-LR and BMAA Confirm Suitability of Aegagropila Linnaei for Use in Green Liver Systems®–A Case Study with Cyanobacterial Toxins.” Aquatic Toxicology 165: 101–108. doi:10.1016/j.aquatox.2015.05.017.
15. H.Esterbauer, and K.H.Cheeseman. 1990. “Determination of Aldehydic Lipid Peroxidation Products: Malonaldehyde and 4-Hydroxynonenal.” Methods in Enzymology 186: 407–421.
16. I.R.Falconer,, M.T.C.Runnegar, T.Buckley, V.L.Huyn, and P.Bradshaw. 1989. “Using Activated Carbon to Remove Toxicity from Drinking Water Containing Cyanobacterial Blooms.” Journal (American Water Works Association) 81: 102–105.
17. D.Giustarini,, I.Dalle-Donne, A.Milzani, P.Fanti, and R.Rossi. 2013. “Analysis of GSH and GSSG After Derivatization with N-Ethylmaleimide.” Nature Protocols 8: 1660–1669. doi:10.1038/nprot.2013.095.
18. M.Gugger,, S.Lenoir, C.Berger, A.Ledreux, J.C.Druart, J.F.Humbert, C.Guette, and C.Bernard. 2005. “First Report in a River in France of The Benthic Cyanobacterium Phormidium Favosum Producing Anatoxin-a Associated with Dog Neurotoxicosis.” Toxicon 45: 919–928. doi:10.1016/j.toxicon.2005.02.031.
19. M.H.Ha,, V.Contardo-Jara, and S.Pflugmacher. 2014. “Uptake of The Cyanobacterial Neurotoxin, Anatoxin-a, and Alterations in Oxidative Stress in the Submerged Aquatic Plant Ceratophyllum Demersum.” Ecotoxicology and Environmental Safety 101: 205–212. doi:10.1016/j.ecoenv.2013.12.023.
20. M.H.Ha,, and S.Pflugmacher. 2013. “Time-Dependent Alterations in Growth, Photosynthetic Pigments and Enzymatic Defense Systems of Submerged Ceratophyllum Demersum During Exposure to The Cyanobacterial Neurotoxin Anatoxin-a.” Aquatic Toxicology 138: 26–34. doi:10.1016/j.aquatox.2013.04.007.
21. W.H.Habig,, M.J.Pabst, and W.B.Jakoby. 1974. “Glutathione S-Transferases - First Enzymatic Step in Mercapturic Acid Formation.” Journal of Biological Chemistry 249: 7130–7139.
22. R.P.Herbst, 1969. “Ecological Factors and the Distribution of Cladophora Glomerata in The Great Lakes.” The American Midland Naturalist 82: 90–98. doi:10.2307/2423819.
23. W.P.Inskeep,, and P.R.Bloom. 1984. “Comparative study of soil solution chemistry associated with chlorotic and nonchlorotic soybeans in western Minnesota.” Journal of Plant Nutrition 7: 513–531.
24. W.P.Inskeep,, and P.R.Bloom. 1985. “Extinction Coefficients of Chlorophyll a and b in N,N-Dimethylformamide and 80% Acetone.” Plant Physiology 77 (2): 483–485.
25. S.Jana,, and M.A.Choudhuri. 1981. “Glycolate Metabolism of Three Sub-Merged Aquatic Angiosperms During Aging.” Aquatic Botany 12: 345–354. doi:10.1016/0304-3770(82)90026-2.
26. A.Kaminski,, B.Bober, E.Chrapusta, and J.Bialczyk. 2014. “Phytoremediation of Anatoxin-a by Aquatic Macrophyte Lemna Trisulca L.” Chemosphere 112: 305–310. doi:10.1016/j.chemosphere.2014.04.064.
27. T.W.Lambert,, C.F.B.Holmes, and S.E.Hrudey. 1996. “Adsorption of Microcystin-LR by Activated Carbon and Removal in Full Scale Water Treatment.” Water Research 30: 1411–1422. doi:10.1016/0043-1354(96)00026-7.
28. R.C.Lorenz,, M.E.Monaco, and C.E.Herdendorf. 1991. “Minimum Light Requirements of Substrate Colonization by Cladophora Glomerata.” Journal of Great Lakes Research 17: 536–542. doi:10.1016/S0380-1330(91)71389-0.
29. S.M.Mitrovik,, S.Pflugmacher, K.J.James, and A.Furey. 2004. “Anatoxin-a Elicits an Increase in Peroxidase and Glutathione S-Transferase Activity in Aquatic Plants.” Aquatic Toxicology 68: 185–192.
30. M.Muntisov,, and P.Trimboli. 1996. “Removal of Algal Toxins Using Membrane Technology.” Water 23 (3): 34.
31. K.Murugan,, and S.R.Harish. 2007. “Antioxidant Modulation in Response to Heavy Metal Induced Oxidative Stress in Cladophora Glomerata.” Indian Journal of Experimental Biology 45: 980–983.
32. Y.Nakano,, and K.Asada. 1981. “Hydrogen Peroxide is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts.” Plant and Cell Physiology 22: 867–880.
33. B.C.Nicholson,, J.Rositano, and M.D.Burch. 1994. “Destruction of Cyanobacterial Peptide Hepatotoxins by Chlorine and Chloramine.” Water Research 28: 1297–1303. doi:10.1016/0043-1354(94)90294-1.
34. J.Nimptsch,, and S.Pflugmacher. 2005. “Substrate Specificities of Cytosolic Glutathione-S Transferases in Five Different Species of The Aquatic Macrophyte Myriophyllum.” Journal of Applied Botany and Food Quality 79 (2): 94–99.
35. J.Nimptsch,, C.Wiegand, and S.Pflugmacher. 2008. “Cyanobacterial Toxin Elimination via Bioaccumulation of MC-LR in Aquatic Macrophytes: An Application of the “Green Liver Concept”.” Environmental Science and Technology 42: 8552–8557.
36. A.E.Orchard, 1981. “A Revision of South American Myriophyllum (Haloragaceae), and its Repercussion on Some Australian and North American Species.” Brunonia 4: 27–65. doi:10.1071/BRU9810027.
37. H.W.Pearl,, and J.Huisman. 2008. “Blooms Like it Hot.” Science 320: 57–58. doi:10.1126/science.1155398.
38. A.Peuthert,, S.Chakrabarti, and S.Pflugmacher. 2007. “Uptake of Microcystins-LR and -LF (Cyanobacterial Toxins) in Seedlings of Several Important Agricultural Plant Species and the Correlation with Cellular Damage (Lipid Peroxidation).” Environmental Toxicology 22 (4): 436–442. doi:10.1002/tox.20266
39. A.Peuthert,, L.Kun, S.Baik, and S.Pflugmacher. 2015. “Transfer of Cyanobacterial Toxins into Edible Plants via Irrigation with Lake Water - A Chinese Case Study.” Aperito Journal of Aquatic and Marine Ecosystems 1 (1). http://dx.doi.org/10.14437/AJAME-1-101. doi: 10.14437/AJAME-1-101.
40. S.Pflugmacher, 2002. “Possible Allelophathic Effects of Cyanotoxins with Reference to Microcystin-LR in Aquatic Ecosystems.” Environmental Toxicology 17: 407–413. doi 10.1002/tox.10071.
41. S.Pflugmacher, 2004. “Promotion of Oxidative Stress in The Aquatic Macrophyte Ceratophyllum Demersum During Biotransformation of the Cyanobacterial Toxin Microcystin-LR.” Aquatic Toxicology 70 (3): 169–178. doi:10.1016/j.aquatox.2004.06.010
42. S.Pflugmacher, 2015. “Green Liver Concept and Green Liver Systems – a Sustainable Way for Future Water Purification.” Aperito Journal of Aquatic Marine Ecosystems 1 (1): 102. doi:10.14437/AJAME-1-102.
43. S.Pflugmacher,, M.Aulhorn, and B.Grimm. 2007. “Influence of a Cyanobacterial Crude Extract Containing Microcystin-LR on the Physiology and Antioxidative Defence Systems of Different Spinach Variants.” New Phytology 175: 482–489. doi:10.1111/j.1469-8137.2007.02144.x.
44. S.Pflugmacher,, S.Kühn, H.Lee, J.W.Choi, S.Baik, K.S.Kwon, and V.Contardo-Jara. 2015. “Green Liver Systems® for Water Purification – Using the Phytoremediation Potential of Aquatic Macrophytes for the Removal of Different Cyanobacterial Toxins from Water.” American Journal of Plant Science 6: 1607–1618. doi:10.4236/ajps.2015.69161.
45. S.Pflugmacher,, C.Wiegand, K.A.Beattie, G.A.Codd, and C.E.W.Steinberg. 1998. “Uptake of The Cyanobacterial Hepatotoxin Microcystin-LR by Aquatic Macrophytes.” Journal of Applied Botany 72: 228–232.
46. S.Pflugmacher,, C.Wiegand, K.A.Beattie, E.Krause, C.E.W.Steinberg, and G.A.Codd. 2001. “Uptake, Effects, and Metabolism of Cyanobacterial Toxins in the Emergent Reed Plant Phragmites Australis (cav.) Trin. ex Steud.” Environmental Toxicology and Chemistry 20 (4): 846–852.
47. C.Pietsch,, C.Wiegand, M.V.Ame, A.Nicklisch, D.Wunderlin, and S.Pflugmacher. 2001. “The Effects of a Cyanobacterial Crude Extract on Different Aquatic Organisms: Evidence for Cyanobacterial Toxin Modulating Factors.” Environmental Toxicology 16: 535–542. doi:10.1002/tox.10014.
48. C.E.R.Pitcairn,, and H.A.Hawkes. 1973. “The Role of Phosphorus in The Growth of Cladophora.” Water Research 7: 159–162. doi:10.1016/0043-1354(73)90160-7.
49. D.Planas,, S.C.Maberly, and J.E.Parker. 1996. “Phosphorus and Nitrogen Relationships in Cladophora Glomerata in Two Lake Basins of Different Trophic Status.” Freshwater Biology 35: 609–622. doi:10.1111/j.1365-2427.1996.tb01772.x
50. J.Pütter, 1974. “Peroxidases.” In Methods of Enzymatic Analysis, edited by H.U.Bergmeyer, Vol. 2, USA: Academic Press.
51. J.Rositano,, B.Nicholson, and P.Pieronne. 1998. “Destruction of Cyanobacterial Toxins by Ozone.” Ozone Science and Engineering 20: 223–238. doi:10.1080/01919519808547273.
52. H.Sandermann, 1992. “Plant-Metabolism of Xenobiotics.” Trends in Biochemical Science 17: 82–84. doi:10.1016/0968-0004(92)90507-6.
53. S.Saqrane,, I.E.Ghazali, Y.Ouahid, M.E.Hassni, I.E.Hadrami, L.Bouarab, F.F.del Campo, B.Oudra, and V.Vasconcelos. 2007. “Phytotoxic Effects of Cyanobacteria Extract on the Aquatic Plant Lemna Gibba: Microcystin Accumulation, Detoxication and Oxidative Stress Induction.” Aquat Toxicology 83 (4): 284–294. doi:10.1016/j.aquatox.2007.05.004.
54. S.Singh,, P.K.Rai, R.Chau, A.K.Ravi, B.A.Neilan, and R.K.Asthana, 2015. “Temporal Variations in Microcystin-Producing Cells and Microcystin Concentrations in Two Freshwater Ponds.” Water Research 69: 131–142. doi:10.1016/j.watres.2014.11.015.
55. M.O.Skulberg,, G.A.Codd, and W.W.Carmichael. 1984. “Toxic Blue- Green Algae in Portuguese Freshwaters.” Archives of Hydrobiology 130 (4): 439–451.
56. J.Stüven,, and S.Pflugmacher. 2007. “Antioxidative Stress Response of Lepidium Sativum Due to Exposure to Cyanobacterial Secondary Metabolites.” Toxicon 50 (1): 85–93. doi:10.1016/j.toxicon.2007.02.019.
57. J.Weiss,, H.P.Liebert, and W.Braune. 2000. “Influence of Microcystin-RR on Growth and Photosynthetic Capacity of The Duckweed Lemna Minor L.” Journal of Applied Botany 74: 100–105.
58. A.R.Wellburn, 1994. “The Spectral Determination of Chlorophyll A and Chlorophyll B, as well as Total Carotenoids, Using Various Solvents with Spectrophotometers of Different Resolution.” Journal of Plant Physiology 144 (3): 307–313. doi:10.1016/S0176-1617(11)81192-2.
59. B.A.Whitton, 1967. “Studies on The Growth of Riverain Cladophora in Culture.” Archives of Microbiology 58: 21–29.
60. B.A.Whitton, 1970. “Toxicity of Zinc, Copper and Lead to Chlorophyta from Flowing Waters.” Archives of Microbiology 72: 353–360. doi:10.1007/BF00409034.
61. K.A.Wilson,, E.T.Howell, and D.A.Jackson. 2006. “Replacement of Zebra Mussels by Quagga Mussels in the Canadian Nearshore of Lake Ontario: The Importance of Substrate, Round Goby Abundance, and Upwelling Frequency.” Journal of Great Lakes Research 32: 11–28. doi:10.3394/0380-1330(2006)32[11:ROZMBQ]2.0.CO;2.
62. L.Yin,, J.Huang, D.Li, and Y.Liu. 2005. “Microcystin-RR Uptake and its Effects on the Growth of Submerged Macrophyte Vallisneria Natans (Lour.) Hara.” Environmental Toxicology 20 (3): 308–313. doi:10.1002/tox.20122.