Browse > Article

Changes in Microcystin Production in Microcystis aeruginosa Exposed to Different Concentrations of Filtered Water from Phytoplanktivorous and Omnivorous Fish  

Jang, Min-Ho (Institute for Environmental Technology and Industry, Pusan National University)
Jung, Jong-Mun (Pusan Water Quality Institute, Waterworks HQ)
Yoon, Ju-Duk (Department of Biology, Pusan National University)
Lee, You-Jeong (Pusan Water Quality Institute, Waterworks HQ)
Ha, Kyong (Institute for Environmental Technology and Industry, Pusan National University)
Publication Information
Abstract
This study was to evaluate microcystin production by Microcystis aeruginosa in response to three different levels of indirect (0, 10, 50% of fish cultured media filtrate; control, FCMF1 and FCMF2) exposures to omnivorous and planktivorous fish (Carassius gibelio langsdorfi and Hypophthalmichthys molitrix, CCMF and HCMF, repectively). The cell biomass, intracellular microcystin (MC) and extracellular MC were measured everyday. The intracellular MC contents of all treatments were significantly increased than the controls (CCMF1, P=0.015; CCMF2, P<0.001; HCMF1, P<0.001; HCMF2, P<0.001). The intracellular MC contents of M. aeruginosa were significantly higher in CCMF2 than in CCMF1 (P=(0.023), Those of M, aeruginosa in HCMF2 were significantly higher than that in HCMF1 (P<0.001). The extracellular MC contents were not significantly different between control and CCMFs but those of M, aeruginosa in HCMF1 and HCMF2 were significantly higher than that in control (HCMF1, P=0.003; HCMF2, P<0.001). This study strongly supports that induced-defensive MC production (intra and extracellular MC) of potentially toxic cyanobacteria in response to kairomone concentration and this results can consider the biomanipulation of eutrophic waters as well as an information concerning strategies for recovering eutrophic waters.
Keywords
Microcystis aeruginosa; Hypophthalmichthys molitrix; Carassius gibelio langsdorfi; intracellular microcystin; extracellular microcystin; kairomones;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Bury, N.R., F.B. Eddy and G.A. Codd. 1995. The effects of cyanobacterium Microcystis aeruginosa, the cyanobacterial hepatotoxin microcystin-LR, and ammonia on growth rate and ionic regulation of brown trout. J. Fish Biol. 46: 1042-1054
2 De Bernardi, R. and G. Giussani. 1990. Are blue-green algae suitable food for zooplankton? A review. Hydrobiologia 200/201: 29-41   DOI
3 Dicke, M. and M.W. Sabelis. 1988. Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct. Ecol. 2: 131-139   DOI   ScienceOn
4 Endler, J.A. 1986. Defense against predators.-In: Feder, M.E. and Lauder, G.V. (eds.), Predator-prey relationships: perspectives and approached from the study of lower vertebrates. Univ. of Chicago, Chicago, p. 109-134
5 Fialkowska, E. and A. Pajdak-Stos. 1997. Inducible defence against a ciliate grazer, Pseudomicrothorax dubius, in two strains of Phormidium (cyanobacteria). Proc. R. Soc. Lond. B. 264: 937-941
6 Harada, K.I., K Matsuura, M. Suzuki, H. Oka, M.F. Watanabe, S. Ohshi, A.M. Dahlem, V.R. Beasley and W.W. Carmichael. 1988. Analysis and purification of toxic peptides from cyanobacteria by reversed-phase high performance liquid chromatography. J. Chromatogr, 448: 275-283   DOI   ScienceOn
7 Jang, M.-H., K. Ha and G.-J. Joo. 2003b. Toxin-mediated between cyanobacteria and native fish in the eutrophic Hoedong Reservoir, South Korea. J. Freshwater Ecol. 18: 639-646   DOI   ScienceOn
8 Jang, M.-H., K. Ha, M.C. Lucas, G.-J. Joo and N. Takamura. 2004. Changes in MC production by Microcystis aeruginosa exposed to phytoplanktovorous and omnivorous fish. Aquat. Toxicol. 68: 51-59   DOI   ScienceOn
9 Kats, L.B. and L.M. Dill. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 4: 361-394
10 Lampert, W. 1987. Laboratory studies on zooplankton-cyanobacteria interactions. New. Zeal. J. Mar. Fresh. 21: 483-490   DOI
11 Lurling, M. and E. van Donk. 1997. Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnol. Oceanogr. 42: 783-788   DOI   ScienceOn
12 Starling, F. 1993. Control of eutrophication by silver carp (Hypophthalmichthys molitrix Valenciennes) in the tropical Pranoa Reservoir (Brasila, Brazil): a mesocosm experiment. Hydrobiologia 257-258: 143-152
13 Wiackowski, K. and A. Starοnska. 1999. The effect of predator and prey density on the induced defence of a ciliate. Funct. Ecol. 13: 59-65   DOI   ScienceOn
14 Wiegand, C., S. Pflugmacher, A. Oberemm, N. Meems, K.A. Beattie, C.E.W. Steinberg and G.A. Codd. 1999. Uptake and effects of microcystin-LR on detoxification enzymes of early life stages of the zebrafish (Danio rerio). Environ. Toxicol. 14: 89-95   DOI
15 Wiegand, C. and S. Pflugmacher. 2005. Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol. Appl. Pharm. 203: 201-218   DOI   ScienceOn
16 Smith, R.J.F. 1997. Avoiding and deterring predators. -In: Godin, J.-G.J. (ed.) Behavioural ecology of teleost fishes. Oxford Univ. Press. Oxford, p. 163-190
17 Williams, D.E., M. Craig, S.C. Dawe, M.L. Kent, R.J. Andersen and C.F.B. Holmes. 1997. ${14}C$ labeled microcystin-LR administered to atlantic salmon via intraperitoneal injection provides in vivo evidence for covalent binding of microcystin- LR in salmon livers. Toxicon 35: 985-989   DOI   ScienceOn
18 Lampert, W., K.O. Rothhaupt and E. von Elert. 1994. Chemical induction of colony formation in a green alga (Scenedesmus acutus) by grazers (Daphnia). Limnol. Oceanogr. 39: 1543-1550   DOI   ScienceOn
19 Jang, M.-H., K. Ha, J.-M. Jung, Y.-J. Lee and N. Takamura. 2006. Increased microcystin production of Microcystis aeruginosa by indirect exposure of nontoxic cyanobacteria: Potential role in the development of Microcystis bloom. Bull. Environ. Contam. Toxicol. 76: 957-962   DOI
20 Jang, M.-H., J.-M. Jung and N. Takamura. 2007b. Changes in microcystin production in cyanobacteria exposed to zooplankton at different population densities and infochemical concentrations. Limnol. Oceanogr. 52(4): 1454 -1466   DOI   ScienceOn
21 Verity, P.G. and V. Smetacek. 1996. Organism life-cycles, predation, and the structure of marine pelagic ecosystems. Mar. Ecol. Prog. Ser. 130: 277-293   DOI
22 Kasai, F., M. Kawachi, M. Erata and M.M. Watanabe. 2004. NIES Collection List of Strains: Microalgae and Protozoa. 7th ed. NIES Environment Agency, Tsukuba, Japan
23 Rapala, J., K. Sivonen, L. Christina and S.I. Niemelä. 1997. Variation of microcystins, cyanobacterial hepatotoxins, in Anabaena spp. As a function of growth stimuli. Appl. Environ. Microbiol. 63: 2206-2212
24 Jang, M.-H., K. Ha, G.-J. Joo and N. Takamura. 2003a. Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biol. 48: 1540-1550   DOI   ScienceOn
25 Fisher, W.J. and D.R. Dietrich. 2000. Pathological and biochemical characterization of Microcystin-induced hepatopancreas and kidney damage in Carp (Cyprinus carpio). Toxicol. Appl. Pharm. 164: 73-81   DOI   ScienceOn
26 Carbis, C.R., G.T. Rawlin, P. Grant, G.F. Mitchell, J.W. Anderson and I. McGauley. 1997. A study of the feral carp, Cyprrinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia and possible implications for fish health. J. Fish Dis. 20: 81-91   DOI   ScienceOn
27 Gliwicz, Z.M. and P. Maszczyk. 2007. Daphnia growth is hindered by chemical information on predation risk at high but not at low food levels. Oecologia 150: 706-715   DOI
28 Lu, K., C. Jin, S. Dong, B. Gu and S.H. Bowen. 2006. Feeding and control of blue-green algal blooms by tilapia (Oreochromis niloticus). Hydrobiologia 568: 111-120
29 Henrikson, B.I. and J.A.E. Stenson. 1993. Alarm substance in Gyrinus aeraus (Coleoptera, Gyrinidae), Oecologia 93: 191-194   DOI
30 DeMott, W.R., Q.X. Zhang and W.W. Carmichael. 1991. Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol. Oceanogr. 36: 1346-1357   DOI   ScienceOn
31 하 경, 장민호, 정종문, 주기재. 2003. 동물플랑크톤 배양여과액에 의한 Microcystis aeruginosa의 성장, 형태 및 microcystin 생성량의 변화. 육수지 36: 1-8
32 Dittmann, E. and T. Borner. 2005. Genetic contributions to the risk assessment of MC in the environment. Toxicol. Appl. Pharm. 203: 192-2000   DOI   ScienceOn
33 Codd, G.A. 1995. Cyanobacterial toxins: occurrence, properties, and biological significance. Water Sci. Technol. 32: 146-159
34 Larrson, P. and S. Dodson. 1993. Chemical communication in planktonic animals. Arch. Hydrobiol. 129: 129-155
35 Oh, H.-M., S.J. Lee, M.-H. Jang and B.-D. Yoon. 2000. MC production by Microcystis aeruginosa in a phosphoruslimited chemostat. Appl. Environ. Microb. 66: 176-179   DOI
36 Zimba, P.V., L. Khoo, P.S. Gaunt, S. Brittain and W.W. Carmichael. 2001. Confirmation of catfish, Ictalurus punctatus (Rafinesque), mortality from Microcystis toxins. J. Fish Dis. 24: 41-47   DOI   ScienceOn
37 Kamjunke, N., K. Schmidt, S. Pflugmacher and T. Mehner. 2002. Consumption of cyanobacteria by roach (Rutilus rutilus): useful or harmful to the fish? Freshwater Bioi. 47: 243-250   DOI   ScienceOn
38 Xie, L., P. Xie, K. Ozawa, T. Honma, A. Yokoyama and H.D. Park. 2004. Dynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environ. Pollut. 127: 431-439   DOI   ScienceOn
39 Brönmark, C. and L.-A. Hansson. 2000. Chemical communication in aquatic systems: an introduction. Oikos 88: 103-109   DOI   ScienceOn
40 Datta, S. and B.B. Jana. 1998. Control of bloom in a tropical lake: grazing efficiency of some herbivorous fishes. J. Fish Biol. 53: 12-24   DOI
41 Haney, J.F., D.J. Forsyth and M.R. James. 1994. Inhibition of zooplankton filtering rates by dissolved inhibitors produced by naturally occurring cyanobacteria. Arch. Hydrobiol. 132: 1-13
42 Bagnaz, D., G. Staaks and C. Steinberg. 1998. Impact of the cyanobacteria toxin, microcystin-LR on behaviour of zebrafish, Dania reria. Water Res. 32: 948-952   DOI   ScienceOn
43 Loose, C.J., E. Von Elert and P. Dawidowicz. 1993. Chemically-induced diel vertical migration in Daphnia: a new bioassay for kairomones exuded by fish. Arch. Hydrobiol. 126: 329-337
44 Parejko, K. and S. Dodson. 1990. Progress towards characterization of a predator/prey kairomone: Daphnia pulex and Chaoborus americanus. Hydrobiologia 198: 51-59   DOI
45 Proulx, M., F.R. Pick, A. Mazumder, P.B. Hamilton and D.R.S. Lean. 1996. Effects of nutrients and planktivorous fish on the phytoplankton of shallow and deep aquatic systems. Ecology 77: 1556-1572   DOI   ScienceOn
46 Jang, M.-H., K. Ha and N. Takamura. 2007a. Reciprocal allelopathic responses between toxic cyanobacteria (Microcystis aeruginosa) and duckweed (Lemna japonica). Toxicon 49: 727-733   DOI   ScienceOn
47 Burks, R.L., E. Jeppesen and D.M. Lodge. 2000. Macrophyte and fish chemicals suppress Daphnia growth and life history traits. Oikos 88: 139-147   DOI   ScienceOn
48 Fisher, W.J., B.C. Hitzfeld, F. Tencalla, J.E. Eriksson, A. Mikhailov and D.R. Dietrich. 2000. Microcystin-LR toxicodynamics, induced pathology, and immunohistochemical localization in livers of blue-green algae exposed rainbow trout (oncorhynchus myiss), Toxicol. Sci. 54: 365-373   DOI   ScienceOn
49 김백호, 김보라, 한명수. 2005. 박테리아와 어류가 유해조류 Microcystis aeruginosa의 성장 및 형태변화에 미치는 영향. 육수지 38: 420-428   과학기술학회마을