Korean Journal of Ecology and Environment (생태와환경)

The Korean Society of Limnology (한국수생태학회)
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Accumulation and Inhibitory Effects of Microcystin on the Growth of Rice and Broccoli

  • Maejima, Kazuhiko (Department of Environmental Sciences, Faculty of Science, Shinshu University) ;
  • Muraoka, Terukazu (Department of Environmental Sciences, Faculty of Science, Shinshu University) ;
  • Park, Ho-Dong (Department of Environmental Sciences, Faculty of Science, Shinshu University)
  • Received : 2013.06.04
  • Accepted : 2013.10.31
  • Published : 2014.02.28
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Abstract

Microcystins (MCs) produced by cyanobacteria are severe hepatotoxins for mammalian and protein phosphatase inhibitors. Irrigation water for grain and vegetables is often contaminated with cyanobacteria and microcystin during warm seasons. We assessed the effects of various concentrations (0, 0.01 to $10{\mu}gmL^{-1}$) of microcystin-LR (MC-LR) and microcystin-RR (MC-RR) exposure on Oryza sativa (rice) and Brassica oleraces var. italica (broccoli). The $EC_{50}$ of leaves and roots of rice was 0.9 and $1.1{\mu}gMC-LRmL^{-1}$, respectively. The no observed effect level (NOEL) of rice was less than $0.1{\mu}gmL^{-1}$ ($100{\mu}gL^{-1}$). The $EC_{50}$ of the stems and roots of broccoli was 8.7 and $7.2{\mu}gMC-RRmL^{-1}$, respectively. There was no difference in the germination rate of broccoli among microcystin-RR concentrations. After exposure to 0, 0.01 to $10{\mu}gmL^{-1}$ MC-RR for seven days, 14, 89 and 154 ng mg-1 (dry weight) MC-RR accumulated in B. oleracea. These $EC_{50}$ values showed that microcystin-LR and -RR affected the growth of rice and broccoli. These findings suggest that MC is carried into terrestrial ecosystems via irrigation, and that the biota of higher ecological niches can be influenced by MC through bioaccumulation. Therefore, a guideline for MC concentrations in irrigation water should be set using the NOEL.

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References

  1. Abe, T., T. Lawson, J.D.B. Weyers and J.A. Codd. 1996. Microcystin-LR inhibits Photosynthesis of Phaselous vulgaris primary leaves: implications for current Spray irrigation practice. New Phytologist 133: 651-658. https://doi.org/10.1111/j.1469-8137.1996.tb01934.x
  2. Amorim, A. and V. Vasconcelos. 1999. Dynamics of microcystins in the mussel Mytilus galloprovincialis. Toxicon 37: 1041-1052. https://doi.org/10.1016/S0041-0101(98)00231-1
  3. Botes, D.P., A.A. Tinman, P.L. Wessels, C.C. Vijoen, H. Kruger, D.H. Williams, S. Santikarn, R.J. Smoth and S.J. Hammond. 1984. The structure of cyanoginosin-LA, a cyclic hepatapeptide toxins from Microcystis aeruginosa. Journal of the Chemical Society Perkin Transactions 1: 2311-2318.
  4. Botes, D.P., H. Kruger and C.C. Viljoen. 1982. Isolation and characterization of four toxins from the blue-green alga, Microcystis aeruginosa. Toxicon 20: 945-954. https://doi.org/10.1016/0041-0101(82)90097-6
  5. Codd, G.A., J.S. Metcalf and K.A. Beattie. 1999. Retention of Microcystis aeruginosa and microcystin by salad lettuce (Lacture sativa) after spray irrigation with water containing cyanobacteria. Toxicon 37: 1181-1185. https://doi.org/10.1016/S0041-0101(98)00244-X
  6. De Maagd, P.G.J., A.J. Hendriks, W. Seinen and D.T.H.M. Sijm. 1999. pH-depended hydrophobicity of the cyanobacteria toxin microcystin-LR. Water Research 33: 677-680. https://doi.org/10.1016/S0043-1354(98)00258-9
  7. Ding, W., H. Shen, H. Zhu, B. Lee and C. Ong. 1999. Genotoxicity of microcystic cyanobacteria extract of a water source in China. Mutation Research 442: 69-77. https://doi.org/10.1016/S1383-5718(99)00064-9
  8. Francis, G. (1878) Poisonous Australian Lake. Nature 18: 11-12.
  9. Galey, F.D., V.R. Beaseley and W.W. Carmichael. 1987. Blue-green algae (Microcystis aeruginosa) hepatotoxicosis in dairy cows. American Journal of Veterinary Research 48, 1415-1420.
  10. Gehringer, M.M., V. Kewada, N. Coates, T.G. Downing. 2003. The use of Lepidium sativum in a plant bioassay system for the detection of microcystin-LR. Toxicon 41: 871-876. https://doi.org/10.1016/S0041-0101(03)00049-7
  11. Gupta, N., S.C. Pant, R. Vijayaraghavan and R.V. Lakshmana Rao. 2003. Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin (LR, RR, YR) in mice. Toxicology 188: 1285-296.
  12. Harada, K.I., K. Tsuji. 1998. Persistence and decomposition of hepatotoxic microcystins produced by cyanobacteria in natural environment. Journal of Toxicology 17: 385-403.
  13. Jianzhong, C., S. Lirong, D. Jian, G. Nanqin and L. Zhili. 2004. Effects of microcystins on the growth and the activity of superoxide dismutase and peroxidase of rape (Brassica napus L.) and rice (Oryza sativa L.). Toxicon 43: 383-400.
  14. Jochimsen, E.M., W.W. Carmichael, J. An, D.M. Cardo, S.T. Cookson, C.E.M. Holmes, M.B. Antunes de C., D.A. Filho de M., T.M. Lyra, V.S.T. Barreto, S.M.F.O. Azevedo and W.R. Jarvis. 1998. Liver failure and death after exposure to microcystins at a heamodialysis center in Brazil. New England Journal of Medicine 338: 873-878. https://doi.org/10.1056/NEJM199803263381304
  15. Jones, G.T. and P.T. Orr. 1994. Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Research 28: 871-876. https://doi.org/10.1016/0043-1354(94)90093-0
  16. Kurki-Helasmo, K. and J. Meriluoto. 1998. Microcystin uptake inhibits growth and protein phosphatase activity in mustard (Sinapis alba L.) seedling. Toxicon 36: 1921-1926. https://doi.org/10.1016/S0041-0101(98)00114-7
  17. Kusumi, T., T. Ooi, M.M. Watanabe, H. Takahashi and H. Kakisawa. 1987. Cyanoviridin-RR, a toxin from the cyanobacterium (Blue-green alga) Microcystis viridis. Tetrahedron Letters 28: 4695-4698. https://doi.org/10.1016/S0040-4039(00)96600-0
  18. Liras, V., M. Lindberg, P. Nystrom, H. Annadotter, L.A. Lawton and B. Graf. 1998. Can ingestied cyanobacteria be harmful to the signal crayfish (Pacifastacus leniusculus)? Freshwater Biology 39: 233-242. https://doi.org/10.1046/j.1365-2427.1998.00278.x
  19. Liu, B., G. Yan, B. Xiao, J. Liu and Y. Liu. 2008. A laboratory study on risk assessment of microcystin-LR in cropland. Journal of Environmental Management 86: 566-574. https://doi.org/10.1016/j.jenvman.2006.12.040
  20. Liu, Y., L. Song, X. Li and T. Liu (2002) The toxic effects of microcystin-LR on embryo-larval and juvenile development of loach, Misguruns mizolepis Gunthe. Toxicon 40: 395-399. https://doi.org/10.1016/S0041-0101(01)00173-8
  21. Liyan, Y., H. Jiaquan, L. Dunhai and L. Yongding. 2005. Microcystin-RR Uptake and effects on the growth of submerged macrophyte Vallisneria natans (lour.) Hara. Environmental Toxicology 20: 308-313. https://doi.org/10.1002/tox.20122
  22. Liyan, Y., H. Jiaquan, L. Wei and L. Yongding. 2006. Microcystin-RR-induced apoptosis in tobacco BY-2 cells. Toxicon 48: 204-210. https://doi.org/10.1016/j.toxicon.2006.05.002
  23. MacKintosh, C., K.A. Beattie, S. Klumpp, P. Cohen and G.A. Codd. 1990. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. Federation of European Biochemical Societies 264: 187-192. https://doi.org/10.1016/0014-5793(90)80245-E
  24. Magalhaes, V.F., M.M. Marinho, P. Domingos, A.C. Oliveira, S.M. Costa, L.O. Azevedo and S.M.F.O. Azevedo. 2003. Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and cruataceans from Sepetiba Bay (Brasil, RJ). Toxicon 42: 289-295. https://doi.org/10.1016/S0041-0101(03)00144-2
  25. Maruyama, T., H.D. Park, A. Yokoyama, T. Tanaka and K. Kato. 2003. Population dynamics of bacteria degrading in a colony of Microcystis. FEMS Microbiology Ecology 46: 279-288. https://doi.org/10.1007/s00248-002-3007-7
  26. Mathe, C., M. M-Hamvas, G. Vasas, G. Suranyi, I. Bacsi, D. Beyer, S. Toth, M. Timar and G. Borbely. 2007. Microcystin-LR, a cyanobacterial toxin, induces growth inhibition and histological alterations in common reed (Phragmites australis) plants regenerated from embryogenic calli. New Phytologist 176: 824-835. https://doi.org/10.1111/j.1469-8137.2007.02230.x
  27. McElhiney, J., L.A. Lawton and C. Leifert. 2001. Investigations into the inhibitory effects of microcystins on plant growth, and the toxity of plant tissues following exposure. Toxicon 39: 1411-1421. https://doi.org/10.1016/S0041-0101(01)00100-3
  28. M-Hamvas, M., C. Mathe, E. Molnar, G. Vasas, I. Grigorszky and G. Borbely. 2002. Microcystin-LR alters the growth, anthocyanin contnt and single-stranded DNase enzyme ativities in Sinapis alba L. seedlings. Aquatic Toxicology 62: 1-9.
  29. Mitrovic, S.M., O. Allis, A. Furrey and K.J. James. 2005. Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Chladophora fracta. Ecotoxicology and Environmental Safety 61: 345-352. https://doi.org/10.1016/j.ecoenv.2004.11.003
  30. Nishiwaki-Matsushima, R., S. Nishiwaki, T. Ohta, S. Yoshizawa, M. Sugaanuma, K.-I. Harada, M.F. Watanabe and H. Fujiki. 1991. Structure-function relationships of microcystins, liver tumor promoters, in intrraction with protein phosphatase. Japanese Journal of Cancer Research 82: 993-996. https://doi.org/10.1111/j.1349-7006.1991.tb01933.x
  31. Nishiwaki-Matsushima, R., T. Ohta, S. Nishiwaki, M. Suganuma, K. Kohyama, T. Ishikawa, W.W. Carmichael and H. Fujiki. 1992. Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. Journal of Cancer Research and Clinical Oncology 118: 420-424. https://doi.org/10.1007/BF01629424
  32. Orr, P.T., G. Jones, R.A. Hunter and K. Berger. 2003. Exposure of beef cattle to sub-clinical doses of Microcystis aeruginosa: toxin bioaccumulation, physiological effects and human risk assessment. Toxicon 41: 613-620. https://doi.org/10.1016/S0041-0101(03)00006-0
  33. Ozawa, K., A. Yokoyama, K. Ishikawa, M. Kumagai, M.F. Watanabe and H.D. Park. 2003. Accumulation and depuration of microcystin produced by cyanobacteria Microcystis in freshwater snail. Limnology 4: 131-138. https://doi.org/10.1007/s10201-003-0106-1
  34. Park, H.D., C. Iwami, M.F. Watanabe, K.I. Harada, T. Okino and H. Hayashi. 1998. Temporal variabilities of the concentrations of intra- and extracellular microcystin and toxic Microcystis Species in a hypertrophic lake, Lake Suwa, Japan (1991-1994). Environmental Toxicology and Water Quality 13: 61-72. https://doi.org/10.1002/(SICI)1098-2256(1998)13:1<61::AID-TOX4>3.0.CO;2-5
  35. Park, H.D., A. Yokoyama and T. Okino. 2001. Fate of microcystin in Lake Suwa (in Japanese). Japanese Journal of Limnology 62: 229-248. https://doi.org/10.3739/rikusui.62.229
  36. Pflugmacher, S. 2002. Possible allelopathic effects of cyanotoxins, with reference to microcystin-LR, in aquatic ecosystems. Environmental Toxicology 17: 407-413. https://doi.org/10.1002/tox.10071
  37. Pflugmacher, S., 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: 846-852. https://doi.org/10.1002/etc.5620200421
  38. Pflugmacher, S., G.A. Codd and C.E.W. Steinberg. 1999. Effects of the cyanobacterial toxin microcystin-LR on detoxification enzymes in aquatic plants. Environmental Toxicology 14: 111-115. https://doi.org/10.1002/(SICI)1522-7278(199902)14:1<111::AID-TOX14>3.0.CO;2-3
  39. Pflugmacher, S., 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 Phytologist 175: 482-489. https://doi.org/10.1111/j.1469-8137.2007.02144.x
  40. Rakwel, R., K. Shii, G.K. Agrawal and M. Yonekura. 2001. Protein phosphatase inhibitors activate defense responses in rice (Oryza sativa) leaves. Physiologia Plantarum 111: 151-157. https://doi.org/10.1034/j.1399-3054.2001.1110204.x
  41. Rinehart, K.L., M. Namikoshi and B.W. Choi. 1994. Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). Journal of Applied Phycology 6: 159-176. https://doi.org/10.1007/BF02186070
  42. Rohrlack, T., E. Dittmann, T. Borner and K. Christffersen. 2001. Effects of cell-bound microcystins on survival and feeding of Daphnia spp. Journal of Applied Environmental Microbiology 67: 3523-3529. https://doi.org/10.1128/AEM.67.8.3523-3529.2001
  43. Saqrane, S., I.E. Ghazali, Y. Ouahid, M.E. Hassni, I.E. Hadrami, L. Bouarab, del F.F. 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. Aquatic Toxicology 83: 284-294. https://doi.org/10.1016/j.aquatox.2007.05.004
  44. Sivonen, K. and J. Jones. 1999. A guide to public health consequence, monitoring and management, p. 55-124. In: Toxic cynaobacteria in water, a guide to public health consequence, monitoring and management (Chorus, I., J.E. Bartram and F.N. Spon, eds.). London.
  45. Smith, G.D. and N.T. Doan. 1999. Cyanobacterial metabolites with bioactivity against photosynthesis in cyanobacteria, algae and higher plants. Journal of Applied Phycology 11: 337-344. https://doi.org/10.1023/A:1008115818348
  46. UNESCO. 1966. Determination of photosynthetic pigments in sea-water. Monographs on Oceanographic Methodology 1: 1-69.
  47. Vaconcelos, V., S. Oliveira and F.O. Teles. 2001. Impact of a toxic and a non-toxic strain of Microcystis aeruginosa on the crayfish Procambarus clarkia. Toxicon 39: 1461-1470. https://doi.org/10.1016/S0041-0101(01)00105-2
  48. Vasconcelos, V.M. 1995. Uptake and depuration of the heptapeptide toxin microcystin-LR in Mytilus galloprovincialis. Aquatic Toxicology 32: 227-237. https://doi.org/10.1016/0166-445X(94)00085-5
  49. Watanabe, M.F., K.I. Harada and H. Fujiki. 1994. Waterbloom of blue-green algae and their toxins. Tokyo: University of Tokyo Press. pp. 257 (Japanese).
  50. Weiss, J., H.P. Libert 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.
  51. WHO. 1998. Guidelines for drinking water quality, Second edition, addendum to volume 2, Health criteria and other supporting information. World Health Organization, Geneva.
  52. Wiegand, C., A. Peuthert, S. Pflugmather and S. Carmeli. 2002. Effects of microcin SF608 and microcystin-LR, two cyanobacterial compounds produced by Microcystis sp., on aquatic organism. Environmental Toxicology 17: 400-406. https://doi.org/10.1002/tox.10065
  53. Williams, D.E., S.C. Dawe, M.L. Kent, R.J. Andersen, M. Craig and C.F.D. Holmes. 1997. Bioaccumulation and clearance of microcystins from salt water mussels, Mytilus Edulis, and in vivo evidence for covalently bound microcystins in mussel tissues. Toxicon 35: 1617-1625. https://doi.org/10.1016/S0041-0101(97)00039-1
  54. Xie, L., P. Xie, K. Ozawa, T. Honma, A. Yokoyama and H.D. Park. 2004. Dynamics of microcystin-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environmental Pollution 127: 431-439. https://doi.org/10.1016/j.envpol.2003.08.011
  55. Yokoyama, A. and H.D. Park. 2003. Depuration and kinetics and persistence of the cyanobacterial toxin microcystin-LR in the freshwater bivalve Unio douglasiae. Environmental Toxicology 18: 61-67. https://doi.org/10.1002/tox.10102
  56. Yoshizawa, S., R. Matsushima, M.F. Watanabe, K.I. Harada, A. Ichihara, W.W. Carmichael and H. Fujiki. 1990. Inhibition of protein phosphatases by microcystin and nodularin associated with hepatotoxicity. Journal of Cancer Research and Clinical Oncology 116: 609-614. https://doi.org/10.1007/BF01637082
  57. Zimba, P.V., L. Khoo, P.S. Graunt, S. Britain and W.W. Carmichael. 2001. Confirmation of catfish, Ictalurus punctatus (Rafinesque) mortality from Microcystis toxins. Journal of Fish Diseases 24: 41-47. https://doi.org/10.1046/j.1365-2761.2001.00273.x
  58. Zurawell, R.W., H. Chen, J.M. Burke and E.E. Prepas. 2005. Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. Journal of Toxicology and Environmental Health, Part B: Critical Reviews 8: 1-37. https://doi.org/10.1080/10937400590889412