Occurrence of Microcystin-Containing Toxic Water Blooms in Central India

  • Agrawal Manish K. (Department of Biological Sciences, Rani Durgavati University) ;
  • Ghosh Shubhro K. (Department of Biological Sciences, Rani Durgavati University) ;
  • Bagchi Divya (Department of Biological Sciences, Rani Durgavati University) ;
  • Weckesser Juergen (Institut fur Biologie II, Mikrobiologie, Albert-Ludwigs Universitat) ;
  • Erhard Marcel (AnagnosTec GmbH) ;
  • Bagchi Suvendra N. (Department of Biological Sciences, Rani Durgavati University)
  • 발행 : 2006.02.01

초록

Three out of fourteen Microcystis-dominant cyanobacterial blooms in Central India were found to be toxic to mice ($LD_{50}$ ranging from 35-450 mg bloom dry mass/kg body weight). The liver architecture of the treated mice showed characteristic symptoms of hepatotoxicity relative to the untreated controls, with increased enzyme activities of serum lactate dehydrogenase (LDH), serum glutamate oxaloacetate transaminase (SGOT), alkaline phosphatase (ALP), and serum glutamate pyruvate transaminase (SGPT). RP-HPLC revealed the presence of microcystin-LR, microcystin-RR, and desmethyl microcystin-RR in the given region to maximum amounts of 390, 1,030, and $860{\mu}g/g$ bloom dry weight, respectively, corresponding to a maximum of 2.8 mg/l microcystin-LR in the lake water. Further confirmation of the microcystin variants was conducted using a MALDI-TOF MS analysis.

키워드

참고문헌

  1. Agrawal, M. K., D. Bagchi, and S. N. Bagchi. 2001. Acute inhibition of protease and suppression of growth in zooplankter, Moina macrocopa, by Microcystis blooms collected in Central India. Hydrobiologia 464: 37-44 https://doi.org/10.1023/A:1013946514556
  2. Bhattacharya, R., K. Sugendran, R. S. Dangi, and P. V. L. Rao. 1997. Toxicity evaluation of freshwater cyanobacterium Microcystis aeruginosa PCC 7806: II Nephrotoxicity in rats. Biomed. Environ. Sci. 10: 93-101 https://doi.org/10.1159/000016036
  3. Botha, N., M. van de Venter, T. G. Downing, E. G. Shephard, and M. M. Gehringer. 2004. The effect of intraperitoneally administered microcystin-LR on the gastrointestinal tract of Balb/c mice. Toxicon 43: 251-254 https://doi.org/10.1016/j.toxicon.2003.11.026
  4. Carmichael, W. W. 1997. The cyanotoxins. Adv. Bot. Res. 27: 211-256 https://doi.org/10.1016/S0065-2296(08)60282-7
  5. Cuvin-Aralar, M. L., J. Fastner, U Focken, K. Becker, and E. V. Aralar. 2002. Microcystins in natural blooms and laboratory cultured Microcystis aeruginosa from Laguna de Bay, Philippines. Syst. Appl. Microbiol. 25: 179-182 https://doi.org/10.1078/0723-2020-00102
  6. Dhaulakhandi, D. B., K. B. Ahluwalia, P. Poduval, and A. K. Ravi. 2004. Comparative RAPD analysis of causative agent of rhinosporidiosis and Microcystis isolated from pond waters. Curr. Sci. 86: 386-388
  7. Ding W. X., H. M. Shen, and C. N. Ong. 2001. Critical role of reactive oxygen species formation in microcystin-induced cytoskeleton disruption in primary cultured hepatocytes. Toxicol. Environ. Health 64: 507-519 https://doi.org/10.1080/152873901753215966
  8. Erhard, M., H. von Dohren, and P. Jungblut. 1997. Rapid typing and elucidation of new secondary metabolites of intact cyanobacteria using MALDI-TOF mass spectrometry. Nature Biotech. 15: 906-909 https://doi.org/10.1038/nbt0997-906
  9. Gehringer, M. M. 2004. Microcystin-LR and okadaic acid-induced cellular effects: A dualistic response. FEBS Lett. 557: 1-8 https://doi.org/10.1016/S0014-5793(03)01447-9
  10. Gupta, N., S. C. Pant, R. Vijayraghavan, and P. V. L. Rao. 2003. Comparative toxicity evalution 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
  11. Jakobi, C., K. L. Rinehart, G. A. Codd, I. Carmienke, and J. Weckesser. 1996. Occurrence of toxic water blooms containing microcystins in a German lake over a three-year period. Syst. Appl. Microbiol. 19: 249-254 https://doi.org/10.1016/S0723-2020(96)80051-8
  12. Jochimsen, E. M., W. W. Carmichael, J. An, D. M Cardo, S. T. Cookson, E. M. H. Christianne, M. B. D. C. Antunes, D. A. D. Filho, 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 haemodialysis center in Brazil. N. Engl. J. Med. 338: 873-878 https://doi.org/10.1056/NEJM199803263381304
  13. Lawton, L. A., C. Edwards, and G. A. Codd. 1994. Extraction and high performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119: 1525-1530 https://doi.org/10.1039/an9941901525
  14. Lee, T. H., Y. M. Chen, and H. N. Chou. 1998. First report of microcystins in Taiwan. Toxicon 36: 247-255 https://doi.org/10.1016/S0041-0101(97)00128-1
  15. 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 Lett. 264: 187-192 https://doi.org/10.1016/0014-5793(90)80245-E
  16. Marwah, J. B., T. M. Shakila, N. S. Rao, and S. N. Bagchi. 1995. Detoxification of a local Microcystis bloom by an algicidal metabolite from Oscillatoria late-virens. Ind. J. Exp. Biol. 33: 97-100
  17. Neumann, U., V. Campos, S. Cantarero, H. Urrutia, R. Heinze, J. Weckesser, and M. Erhard. 2000. Co-occurrence of non-toxic (cyanopeptolin) and toxic (microcystin) peptides in a bloom of Microcystis sp. from a Chilean lake. Syst. Appl. Microbiol. 23: 191-197 https://doi.org/10.1016/S0723-2020(00)80004-1
  18. Nishiwaki-Matsushima, R., T. Ohta, S. Nishiwaki, M. Suganuma, K. Kohyama, T. Ishikawa, W. W. Carmichael, and H. Fujiki. 1992. Liver tumour promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J. Can. Res. Clin. Oncol. 118: 420-424 https://doi.org/10.1007/BF01629424
  19. Ohtake, A., M. Shirai, T. Aida, N. Mori, K. Harada, K. Matsuura, M. Suzuki, and M. Nakano. 1989. Toxicity of Microcystis species isolated from natural blooms and purification of the toxin. Appl. Environ. Microbiol. 55: 3202-3207
  20. Orr, P. T. and G. J. Jones. 1998. Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol. Oceanogr. 43: 1604-1614 https://doi.org/10.4319/lo.1998.43.7.1604
  21. Parker, D. L., H. D. Kumar, L. C. Rai, and J. B. Singh. 1997. Potassium salts inhibit growth of the cyanobacteria Microcystis spp. in pond water and defined media: Implications for control of microcystin-producing aquatic blooms. Appl. Environ. Biol. 63: 2324-2329
  22. Picanco, M. R., R. M. Soares, V. R. Cagido, S. M. Azevedo, P. R. Rocco, and W. A. Zin. 2004. Toxicity of a cyanobacterial extract containing microcystins to mouse lungs. Braz. J. Med. Res. 37: 1225-1229 https://doi.org/10.1590/S0100-879X2004000800013
  23. Ranatala, A., D. P. Fewer, M. Hisbergues, L. Rouhiainen, J. Vaitomaa, T. Borner, and K. Sivonen. 2004. Phylogenetic evidence for the early evolution of microcystin synthesis. Proc. Natl. Acad. Sci. USA 101: 568-573
  24. Rao, P. V. L. and R. Bhattacharya. 1996. The cyanobacterial toxin microcystin-LR induced DNA damage in mouse liver in vivo. Toxicology 114: 29-36 https://doi.org/10.1016/S0300-483X(96)03413-0
  25. Rao, P. V. L., R. Bhattacharya, and S. Dasgupta. 1994. Isolation, culture and toxicity of cyanobacterium (blue-green alga) Microcystis aeruginosa from freshwater source in India. Bull. Environ. Contam. Toxicol. 52: 878-885
  26. Rapala, J., K. Sivonen, C. Lyra, and S. I. Niemela. 1997. Variation of microcystins, cyanobacterial hepatotoxins, in Anabaena spp. as a function of growth stimuli. Appl. Environ. Microbiol. 63: 2206-2212
  27. Shen, P. P., S. W. Zhao, W. J. Zheng, Z. C. Hua, Q. Shi, and Z. T. Liu. 2003. Effects of cyanobacteria bloom extract on some parameters of immune function in mice. Toxicol. Lett. 143: 27-36 https://doi.org/10.1016/S0378-4274(03)00110-3
  28. Sivonen, K. and J. Jones. 1999. Cyanobacterial toxins- A guide to public health significance, monitoring and management, pp. 41-111 In I. Chorus and J. Bartram (eds.), Toxic Cyanobacteria in Water. Spon/Chapman and Hall, London
  29. Ueno, Y., S. Nagata, T. Tsutsumi, A. Hasegawa, M. F. Watanabe, H. D. Park, G. C. Chen, G. Chen, and S. Z. Yu. 1996. Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17: 1317-1321 https://doi.org/10.1093/carcin/17.6.1317
  30. Via-Orodika, L., J. Fastner, R. Kurmayer, M. Hisbergues, E. Dittmann, J. Komarek, M. Erhard, and I. Chorus. 2004. Distribution of microcystin-producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: Detection of microcystins and microcystin genes in individual colonies. Syst. Appl. Microbiol. 27: 592-602 https://doi.org/10.1078/0723202041748163
  31. Vieira, J. M. D. S., M. T. D. P. Azevedo, S. M. D. O. Azevedo, R. Y. Honda, and B. Correa. 2003. Microcystin production by Radiocystis fernandoi (Chroococcales, cyanobacteria) isolated from a drinking water reservoir in the city of Belem, PA, Brazilian Amazonia region. Toxicon 42: 709-713 https://doi.org/10.1016/j.toxicon.2003.08.004
  32. Wang, X., P. Parkpian, N. Fujimoto, K. M. Ruchirawat, R. D. DeLaune, and A. Jugsujinda. 2002. Environmental conditions associating microcystins production to Microcystis aeruginosa in a reservoir of Thailand. J. Environ. Sci. Health A 37: 1181-1207 https://doi.org/10.1081/ESE-120005980
  33. Watanabe, Y., M. F. Watanabe, and M. Watanabe. 1986. The distribution and relative abundance of bloom forming Microcystis species in several eutrophic waters. Jpn. J. Limnol. 47: 87-93 https://doi.org/10.3739/rikusui.47.87
  34. Weil, C. S. 1952. Tables for convenient calculation of median-effective dose $(LD_{50}\;or\;ED_{50})$ and instructions in their use. Biometrics 8: 249-263 https://doi.org/10.2307/3001557
  35. 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
  36. Wirsing, B., T. Flury, C. Weidner, U. Neumann, and J. Weckesser. 1999. Estimation of the microcystin content in field samples from German lakes using the colorimetric protein-phosphatase inhibition assay and RP-HPLC. Environ. Toxicol. Water Qual. 14: 23-29