Korean Journal of Ecology and Environment (생태와환경)

The Korean Society of Limnology (한국수생태학회)
권호 표지
DOI QR코드

DOI QR Code

Microcystins Concentration in Fishes Collected from the Weirs of Four Rivers in Korea and Risk Assessment

국내 4대강 보에서 채집된 어류 조직에서 microcystins 농도 분석 및 위해도 평가

  • Do-Hwan Kim (Department of Environmental Engineering, Chungbuk National University) ;
  • Yuna Shin (Water Quality Assessment Research Division, National Institute of Environmental Research) ;
  • Min Jeong Park (Department of Environmental Engineering, Chungbuk National University) ;
  • Young-Cheol Cho (Department of Environmental Engineering, Chungbuk National University)
  • Received : 2021.12.24
  • Accepted : 2022.04.21
  • Published : 2022.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Microcystins (MCs) are cyano-toxins mainly produced by cyanobacteria in the genera of Microcystis, Anabaena, and Oscillatoria. The concentrations of MCs in the water bodies and fish tissues taken from the four weirs (Ipo, Gangjeong-goryeong, Baekje, and Juksan) in the four main rivers in Korea, and the health risk of human due to consumption of toxin-detected fish was examined. The maximum values of MCs concentration in the water samples were as follows: Juksan (3.261 ㎍ L-1), Gangjeong-goryeong (1.014 ㎍ L-1), Baekje (0.759 ㎍ L-1), and Ipo (0.266 ㎍ L-1) weirs. The MC-RR concentration was the highest among the MCs, and MC-YR was not detected. MCs of 0.222~9.808 ㎍ g-1 dry weight were detected in the liver of 3 out of 215 fishes of 16 species, and below the detection limit in muscle. As a result of comparing the feeding characteristics of the collected fishes and toxin concentrations in water and fish tissue, it was concluded that the biomagnification of MCs through the food chain did not occur. It was judged that there was no health risk due to the consumption of the fish detected the toxin, based on the amount of the fish intake of the Korean people and the allowable daily intake of MCs. However, in order to reduce the health risk due to MCs, further studies should be conducted to analyze the concentration of MCs contained in fish tissues collected at various times in the area dominated by harmful cyanobacteria to obtain data on the exposure of MCs due to fish consumption. In addition, it is necessary to establish the management guidelines for MCs in fish tissues.

Microcystins (MCs)는 남조류독소로 Microcystis, Anabaena, Oscillatoria 속 남조류에 의해 주로 생산된다. 4대강에 있는 4개의 보 (이포보, 강정고령보, 백제보, 죽산보)에서 채집된 수 시료 및 어류 조직에서 MCs의 종류별 농도를 분석하고, 독소가 검출된 어류의 섭취로 인한 인체 위해성을 검토하였다. 수 시료에서 MCs 농도의 최대값은 죽산보(3.261 ㎍ L-1), 강정고령보(1.014 ㎍ L-1), 백 제보 (0.759 ㎍ L-1), 이포보 (0.266 ㎍ L-1)의 순이었으며, MC-RR의 농도가 가장 높았고 MC-YR은 검출되지 않았다. 대상 지역에서 채집된 16종 215개체의 어류 중 3개체의 간에서 0.222~9.808 ㎍ g-1 건조중량의 독소가 검출되 었으며, 나머지 어류의 근육과 간에서는 검출한계 이하였다. 어류의 섭식 특성과 수체 및 어류 조직의 독소 농도를 비교한 결과, MC가 먹이 사슬을 통한 생물증폭은 일어나지 않는 것으로 판단되었다. 한국인의 어류 섭취량과 MCs의 일일 섭취 허용량을 근거로 위해성을 검토한 결과, 독소가 검출된 어류의 섭취로 인한 위해성은 없는 것으로 판단되었다. 하지만 MCs에 의한 위해도를 줄이기 위하여, 추가 연구를 통하여 유해남조류가 우점하는 지역에서 다양한 시기에 채집된 어류의 조직에서 MCs 농도를 분석함으로써 어류 섭취로 인한 MCs의 노출 정도에 대한 자료를 확보하고, 이를 근거로 어류 중 MCs에 대한 관리 기준을 설정하는 것이 필요하다고 사료된다.

Keywords

Acknowledgement

본 연구는 환경부의 연구비 지원에 받아 수행된 연구입니다.

References

  1. Adamovsky, O., R. Kopp, K. Hilscherova, P. Babica, M. Palikova, V. Paskova, S. Navratil, B. Marsalek and L. Blaha. 2007. Microcystin kinetics(bioaccumulation and elimination) and biochemical responses in common carp (Cyprinus carpio) and silver carp (Hypophthalmichthys molitrix) exposed to toxic cyanobacterial blooms. Environmental Toxicology and Chemistry 26: 2687-2693. https://doi.org/10.1897/07-213.1
  2. Ame, M.V., L.N. Galanti, M.L. Menone, M.S. Gerpe, V.J. Moreno and D.A. Wunderlin. 2010. Microcystin-LR, -RR, -YR and -LA in water samples and fishes from a shallow lake in Argentina. Harmful Algae 9(1): 66-73. https://doi.org/10.1016/j.hal.2009.08.001
  3. Amrani, A., H. Nasri, A. Azzouz, Y. Kadi and N. Bouaicha. 2014. Variation in cyanobacterial hepatotoxin (microcystin) content of water samples and two species of fishes collected from a shallow lake in Algeria. Archives of Environmental Contamination and Toxicology 66(3): 379-389. https://doi.org/10.1007/s00244-013-9993-2
  4. Bieczynski, F., V.A. Bianchi and C.M. Luquet. 2013. Accumulation and biochemical effects of microcystin-LR on the patagonian pejerrey (Odontesthes hatcheri) fed with the toxic cyanobacteria Microcystis aeruginosa. Fish Physiology and Biochemistry 39(5): 1309-1321. https://doi.org/10.1007/s10695-013-9785-7
  5. Bouaicha, N., C.O. Miles, D.G. Beach, Z. Labidi, A. Djabri, N.Y. Benayache and T. Nguyen-Quang. 2019. Structural diversity, characterization and toxicology of microcystins. Toxins 11(12): 714.
  6. Burch, M.D. 2008. Effective doses, guidelines and regulations. Advances in Experimental Medicine and Biology 619: 831-853. https://doi.org/10.1007/978-0-387-75865-7_36
  7. California Environmental Protection Agency (California EPA). 2012. Toxicological Summary and Suggested Action Levels to Reduce Potential Adverse Health Effects of Six Cyanotoxins. California Environmental Protection Agency, Sacramento, California, USA.
  8. Campos, A. and V. Vasconcelos. 2010. Molecular mechanisms of microcystin toxicity in animal cells. International Journal of Molecular Sciences 11(1): 268-287. https://doi.org/10.3390/ijms11010268
  9. Carmichael, W.W. 1988. Freshwater cyanobacteria (blue-green algae) toxins, p. 3-16. In: National Toxins Characterization, Pharmacology and Therapeutics., Proceedings of the 9th World Congress on Animal, Plant and Microbial Toxins (Ownby, C.L. and V.G. Odell, eds.). Pergamon Press, New York.
  10. Dai, R., P. Wang, P. Jia, Y. Zhang, X. Chu and Y. Wang. 2016. A review on factors affecting microcystins production by algae in aquatic environments. World Journal of Microbiology and Biotechnology 32(3): 1-7. https://doi.org/10.1007/s11274-015-1971-6
  11. Deblois, C.P., R. Aranda-Rodriguez, A. Giani and D.F. Bird. 2008. Microcystin accumulation in liver and muscle of tilapia in two large Brazilian hydroelectric reservoirs. Toxicon 51(3): 435-448. https://doi.org/10.1016/j.toxicon.2007.10.017
  12. Dyble, J., D. Gossiaux, P. Landrum, D.R. Kashian and S. Pothoven. 2011. A kinetic study of accumulation and elimination of microcystin-LR in yellow perch (Perca flavescens) tissue and implications for human fish consumption. Marine Drugs 9: 2553-2571. https://doi.org/10.3390/md9122553
  13. Falconer, I., J. Bartram, I. Chorus, T. Kuiper-Goodman, H. Utkilen, M. Burch and G.A. Codd. 1999. Safe levels and safe practices, p. 148-169. In: Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management (Chorus, I. and J. Bartram, eds.). Spon Press, London, UK.
  14. Foss, A.J., J. Butt, S. Fuller, K. Cieslik, M.T. Aubel and T. Wertz. 2017. Nodularin from benthic freshwater periphyton and implications for trophic transfer. Toxicon 140: 45-59. https://doi.org/10.1016/j.toxicon.2017.10.023
  15. Geada, P., R.N. Pereira, V. Vasconcelos, A.A. Vicente and B.D. Fernandes. 2017. Assessment of synergistic interactions between environmental factors on Microcystis aeruginosa growth and microcystin production. Algal Research 27: 235-243. https://doi.org/10.1016/j.algal.2017.09.006
  16. Greer, B., R. Maul, K. Campbell and C.T. Elliott. 2017. Detection of freshwater cyanotoxins and measurement of masked microcystins in tilapia from Southeast Asian aquaculture farms. Analytical and Bioanalytical Chemistry 409(16): 4057-4069. https://doi.org/10.1007/s00216-017-0352-4
  17. Gupta, N., S.C. Pant, R. Vijayaraghavan and P.V.L. Rao. 2003. Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. Toxicology 188: 285-296. https://doi.org/10.1016/S0300-483X(03)00112-4
  18. Health Canada. 2012. Guidelines for Canadian Recreational Water Quality, Third Edition. Health Canada, Ottawa, Ontario, Canada.
  19. Honkanen, R.E., J.E.M.R. Zwiller, R.E. Moore, S.L. Daily, B.S. Khatra, M. Dukelow and A.L. Boynton. 1990. Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. The Journal of Biological Chemistry 265(32): 19401-19404.
  20. Ibelings, B.W., K. Bruning, J. de Jonge, K. Wolfstein, L.M.D. Pires, J. Postma and T. Burger. 2005. Distribution of microcystins in a lake foodweb: no evidence for biomagnification. Microbial Ecololgy 49: 487-500. https://doi.org/10.1007/s00248-004-0014-x
  21. Ito, E., A. Takai, F. Kondo, H. Masui, S. Imanishi and K. Harada. 2002. Comparison of protein phosphatase inhibitory activity and apparent toxicity of microcystins and related compounds. Toxicon 40: 1017-1025. https://doi.org/10.1016/S0041-0101(02)00099-5
  22. Janse, I., W.E.A. Kardinaal, M. Meima, J. Fastner, P.M. Visser and G. Zwart. 2004. Toxic and nontoxic microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Applied and Environmental Microbiology 70(7): 3979-3987. https://doi.org/10.1128/AEM.70.7.3979-3987.2004
  23. Janse, I., W.E.A. Kardinaal, M.K.V. Agterveld, M. Meima, P.M. Visser and G. Zwart. 2005. Contrasting microcystin production and cyanobacterial population dynamics in two Planktothrix dominated freshwater lakes. Environmental Microbiology 7(10): 1514-1524.
  24. Jochimsen, E.M., W.W. Carmichael, J.S. An, D.M. Cardo, S.T. Cookson, C.E. Holmes, M.B. Antunes, D.A. de Melo Filho, T.M. Lyra, V.S. Barreto, S.M. Azevedo and W.R. Jarvis. 1998. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. The New England Journal of Medicine 338(13): 873-878. https://doi.org/10.1056/NEJM199803263381304
  25. Kim, B., H.S. Kim, H.D. Park, K. Choi and J.G. Park. 1999. Microcystin content of cyanobacterial cells in Korean reservoirs and their toxicity. Korean Journal of Limnology 32(4): 288-294.
  26. Kotak, B.G., A.K.Y. Lam, E.E. Prepas and S.E. Hrudey. 2000. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Canadian Journal of Fisheries and Aquatic Sciences 57: 1584-1593. https://doi.org/10.1139/f00-091
  27. Kozlowsky-Suzuki, B., A.E. Wilson and S. Ferrao-Filho Ada. 2012. Biomagnification or biodilution of microcystins in aquatic foodwebs? Meta-analyses of laboratory and field studies. Harmful Algae 18: 47-55. https://doi.org/10.1016/j.hal.2012.04.002
  28. Kuiper-Goodman, T., I. Falconer and J. Fitzgerald. 1999. Human health aspects, p. 112-147. In: Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management (Chorus, I. and J. Bartram, eds.). Spon Press, London, UK.
  29. Lei, H., P. Xie, J. Chen, G. Liang, M. Dai and X. Zhang. 2008. Distribution of toxins in various tissues of crucian carp intraperitoneally injected with hepatotoxic microcystins. Environmental Toxicology and Chemistry 27: 1167-1174. https://doi.org/10.1897/07-522.1
  30. Li, L., P. Xie, L. Guo, Z. Ke, Q. Zhou, Y. Liu and T. Qiu. 2008. Field and laboratory studies on pathological and biochemical characterization of microcystin-induced liver and kidney damage in the phytoplanktivorous bighead carp. Scientific World Journal 8: 121-137. https://doi.org/10.1100/tsw.2008.32
  31. 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. FEBS Letters 264(2): 187-192. https://doi.org/10.1016/0014-5793(90)80245-E
  32. Malbrouck, C., G. Trausch, P. Devos and P. Kestemont. 2003. Hepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus L. Comparative Biochemistry and Physiology - Part C 135: 39-48. https://doi.org/10.1016/S1095-6433(02)00352-5
  33. Metcalf, J.S., K.A. Beattie, S. Pflugmacher and G.A. Codd. 2000. Immuno-cross reactivity and toxicity assessment of conjugation products of the cyanobacterial toxin, microcystin-LR. FEMS Microbiology Letters 189: 155-158. https://doi.org/10.1111/j.1574-6968.2000.tb09222.x
  34. Ministry of Environment (MOE). 2007. Development and Application of Korean Exposure Factors. Ministry of Environment, Korea.
  35. Ministry of Environment (MOE). 2016. Standard Methods for Analysis of Water Pollution. Ministry of Environment, Korea.
  36. Mitsoura, A., I. Kagalou, N. Papaioannou, P. Berillis, E. Mente and T. Papadimitriou. 2013. The presence of microcystins in fish Cyprinus carpio tissues: a histopathological study. International Aquatic Research 5: 8.
  37. Namikoshi, M., K.L. Rinehart, R. Sakai, R.R. Stotts, A.M. Dahlem, V.R. Beasley, W.W. Carmichael and W.R. Evans. 1992. Identification of 12 hepatotoxins from a homer lake bloom of the cyanobacteria Microcystis aeruginosa, Microcystis viridis, and Microcystis wesenbergii: nine new microcystins. The Journal of Organic Chemistry 57: 866-872. https://doi.org/10.1021/jo00029a016
  38. National Institute of Environmental Research (NIER). 2007. A Study on the Production and Behavior of Cyanobacterial Toxin. National Institute of Environmental Research, Incheon, Korea.
  39. National Institute of Environmental Research (NIER). 2013. Ecological Risk Assessment on Biogenic Algal Toxin (Microcystin-LR). National Institute of Environmental Research, Incheon, Korea.
  40. Oh, K.H., D.H. Jeong and Y.C. Cho. 2013. Quantification of toxigenic Microcystis spp. in freshwaters by quantitative real-time PCR based on the microcystin synthetase A. Journal of Microbiology 51(1): 18-24. https://doi.org/10.1007/s12275-013-2354-z
  41. Orihel, D.M., D.F. Bird, M. Brylinsky, H. Chen, D.B. Donald, D.Y. Huang, A. Giani, D. Kinniburgh, H. Kling, B.G. Kotak, P.R. Leavitt, C.C. Nielsen, S. Reedyk, R.C. Rooney, S.B. Watson, R.W. Zurawell and R.D. Vinebrooke. 2012. High microcystin concentrations occur only at low nitrogen-to-phosphorus ratios in nutrient-rich Canadian lakes. Canadian Journal of Fisheries and Aquatic Sciences 69(9): 1457-1462. https://doi.org/10.1139/f2012-088
  42. Papadimitriou, T., I. Kagalou, C. Stalikas, G. Pilidis and I.D. Leonardos. 2012. Assessment of microcystin distribution and biomagnification in tissues of aquatic food web compartments from a shallow lake and evaluation of potential risks to public health. Ecotoxicology 21: 1155-1166. https://doi.org/10.1007/s10646-012-0870-y
  43. Park, H.K. 2007. Survey method relating freshwater phytoplankton for the management of water resources. Journal of Korean Society of Environmental Engineers 29(6): 593-609.
  44. Schmidt, J.R., M. Shaskus, J.F. Estenik, C. Oesch, R. Khidekel and G.L. Boyer. 2013. Variations in the microcystin content of different fish species collected from a eutrophic lake. Toxins(Basel) 5: 992-1009.
  45. Sivonen, K. and G. Jones. 1999. Cyanobacterial toxins, p. 41-111. In: Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management (Chorus, I. and J. Bartram, eds.). Spon Press, London, UK.
  46. Smith, J.L. and J.F. Haney. 2006. Foodweb transfer, accumulation, and depuration of microcystins, a cyanobacterial toxin, in pumpkinseed sunfish (Lepomis gibbosus). Toxicon 48: 580-589. https://doi.org/10.1016/j.toxicon.2006.07.009
  47. US Environmental Protection Agency (US EPA). 2006. Toxicological Reviews of Cyanobacterial Toxins: Microcystins LR, RR, YR and LA. US Environmental Protection Agency, Cincinnati, OH, USA.
  48. Welker, M., M. Brunke, K. Preussel, I. Lippert and H. von Dohren. 2004. Diversity and distribution of Microcystis (cyanobacteria) oligopeptide chemotypes from natural communities studied by single-colony mass spectrometry. Microbiology 150: 1785-1796. https://doi.org/10.1099/mic.0.26947-0
  49. Xie, L. and H.D. Park. 2007. Determination of microcystins in fish tissues using HPLC with a rapid and efficient solid phase extraction. Aquaculture 271: 530-536. https://doi.org/10.1016/j.aquaculture.2007.07.004
  50. Xie, L., P. Xie, L. Guo, L. Li, Y. Miyabara and H.D. Park. 2005. Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environmental Toxicology 20: 293-300. https://doi.org/10.1002/tox.20120
  51. 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): 1-37. https://doi.org/10.1080/10937400590889412