白鲢罗非鱼对微囊藻毒素急性、亚急性毒性响应
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摘要
为了探究不同控藻鱼类对产毒微囊藻的适应机制,为生物操纵的鱼种选择提供依据,研究了白鲢和罗非鱼对微囊藻毒素(MC)的生物富集、降解,及两种鱼对毒素的抗性、解毒机制的差异性.结果发现:在喂食微囊藻实验中,白鲢、罗非鱼对MC日摄入量达到10mg/kg,2种鱼均对MC有较强抗性.微囊藻经鱼摄入后,MC总含量在白鲢、罗非鱼粪便中分别下降到71.5%、6.0%,罗非鱼对MC降解能力远高于白鲢.白鲢和罗非鱼的肝系数分别从(1.19±0.21)%、(2.24±0.19)%下降到(0.79±0.06)%、(1.72±0.07)%,均表现出显著差异性下降(P<0.05).微囊藻毒素在白鲢、罗非鱼肌肉中积累量分别为(1.57±0.31)μg/kg、(10.81±6.52)μg/kg(鲜重)、肝脏中积累量分别为(4.28±1.64)mg/kg、(2.48±0.15)mg/kg(鲜重).MC在白鲢、罗非鱼肌肉、肝脏中的积累量均存在显著差异性(P<0.05).罗非鱼肌肉中毒素含量是白鲢的6.9倍.在微囊藻毒素LR(MC-LR)对白鲢和罗非鱼的急性毒性效应实验中,MC-LR对白鲢、罗非鱼的LD50为270和790μg/kg,罗非鱼对毒素有更强耐受性.喂食毒藻和i.p.注射MC均导致白鲢和罗非鱼肝细胞内脂滴大量出现.2种鱼在MC-LR注射后,谷胱甘肽(GSH)含量均表现出6h内明显下降.6h后两种鱼GSH含量均逐步回升,二者差异显著(p<0.05).实验结果表明,罗非鱼对MC降解能力远高于白鲢.白鲢主要摄食群体微囊藻的群体胶鞘和附着细菌,胞内微囊藻毒素释放量小,白鲢这种摄食机制导致它能以产毒微囊藻为食而受到较轻危害.罗非鱼体内消化酶对微囊藻和MC具较强的消化降解能力;GSH含量及相关酶活性水平高,对体内毒素清除效率高.从食用安全性角度出发,与罗非鱼相比,白鲢是更适合用于控制蓝藻水华的鱼种,可广泛应用于蓝藻水华控制中.
In order to study adaptative mechanisms of sliver carp and tilapia on harmful algal blooms and provide scientific methods of fish species selection in biological manipulation, systematic research was conducted on bioaccumulation, degradation of microcystin and the differences in resistance and detoxification mechanisms on sliver carp(Hypophthalmichthys molitrix) and tilapia(Oreochromis niloticus). In toxic Microcystis feeding experiment, the daily intake of microcystin by sliver carp and tilapia was up to 10 mg/kg body weight. Both fishes show strong resistance to MC. Microcystin concentrations in feces of sliver carp and tilapia after Microcystis intake were significantly decreased to 71.5% and 6.0% respectively(P<0.05). The degradation ability of tilapia to toxic Microcystis and microcystin is much higher than silver carp. The hepatosomatic index of sliver carp and tilapia was significantly decreased from(1.19±0.21)% and(2.24±0.19)% to(0.79±0.06)% and(1.72±0.07)% respectively(P<0.05). Bioaccumulations of MC of the two species were(1.57±0.31) and(10.81±6.52)μg/kg(fresh weight) in the muscle,(4.28±1.64) and(2.48±0.15)mg/kg(fresh weight) in the liver. There were significant differences between MC accumulation in the muscle and liver of each species(P<0.05). Microcystin concentration in the muscle of tilapia was 6.9 times higher than that of silver carp. During the toxic experiment, LD50 of microcystin-LR was 270μg/kg on sliver carp and 790μg/kg on tilapia, which suggested microcystin tolerance of tilapia is stronger than that of sliver carp. Enormous lipid droplets were observed in the liver cell of the two species whether fed with Microcystis or intraperitoneally injected with microcystin. After intraperitoneal injection with microcystin-LR, the content of GSH in the two species showed a significant decrease in 6 h and then increased gradually. Significant difference of GSH content was found between the two species(P<0.05). The results showed that the degradation ability of tilapia to microcystin is much higher than silver carp. Silver carp mainly feeds on the mucilage sheath and adhesion bacteria of colonial Microcystis with small amount of intracellular microcystin released. This mechanism can effectively protect silver carp fed with Microcystis to less damage. The digestive enzymes in tilapia have strong digestion and degradation ability to Microcystis and microcystin, and the high level of GSH content and related enzyme activity ensure efficient detoxification of toxins in vivo. From the view of food safety, compared with tilapia, silver carp is the species which is more suitable and to be widely used for cyanobacteria bloom control.
In order to study adaptative mechanisms of sliver carp and tilapia on harmful algal blooms and provide scientific methods of fish species selection in biological manipulation, systematic research was conducted on bioaccumulation, degradation of microcystin and the differences in resistance and detoxification mechanisms on sliver carp(Hypophthalmichthys molitrix) and tilapia(Oreochromis niloticus). In toxic Microcystis feeding experiment, the daily intake of microcystin by sliver carp and tilapia was up to 10 mg/kg body weight. Both fishes show strong resistance to MC. Microcystin concentrations in feces of sliver carp and tilapia after Microcystis intake were significantly decreased to 71.5% and 6.0% respectively(P<0.05). The degradation ability of tilapia to toxic Microcystis and microcystin is much higher than silver carp. The hepatosomatic index of sliver carp and tilapia was significantly decreased from(1.19±0.21)% and(2.24±0.19)% to(0.79±0.06)% and(1.72±0.07)% respectively(P<0.05). Bioaccumulations of MC of the two species were(1.57±0.31) and(10.81±6.52)μg/kg(fresh weight) in the muscle,(4.28±1.64) and(2.48±0.15)mg/kg(fresh weight) in the liver. There were significant differences between MC accumulation in the muscle and liver of each species(P<0.05). Microcystin concentration in the muscle of tilapia was 6.9 times higher than that of silver carp. During the toxic experiment, LD50 of microcystin-LR was 270μg/kg on sliver carp and 790μg/kg on tilapia, which suggested microcystin tolerance of tilapia is stronger than that of sliver carp. Enormous lipid droplets were observed in the liver cell of the two species whether fed with Microcystis or intraperitoneally injected with microcystin. After intraperitoneal injection with microcystin-LR, the content of GSH in the two species showed a significant decrease in 6 h and then increased gradually. Significant difference of GSH content was found between the two species(P<0.05). The results showed that the degradation ability of tilapia to microcystin is much higher than silver carp. Silver carp mainly feeds on the mucilage sheath and adhesion bacteria of colonial Microcystis with small amount of intracellular microcystin released. This mechanism can effectively protect silver carp fed with Microcystis to less damage. The digestive enzymes in tilapia have strong digestion and degradation ability to Microcystis and microcystin, and the high level of GSH content and related enzyme activity ensure efficient detoxification of toxins in vivo. From the view of food safety, compared with tilapia, silver carp is the species which is more suitable and to be widely used for cyanobacteria bloom control.
引文
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[31]Al-Ghais S M.Acetylcholinesterase,glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish[J].Marine Pollution Bulletin,2013,74(1)183-186.
[32]Wang Y C,Jiang L,Li Y F,et al.Excessive selenium supplementation induced oxidative stress and endoplasmic reticulum stress in Chicken Spleen[J].Biological Trace Element Research,2016,172(2):481-487.
[33]Bliss C I.Some principles of bioassay[J].American Scientist,1957,45(5):449-466.
[34]Deng Y,Wang W,Yu P F,et al.Comparison of taurine,GABA,Glu,and Asp as scavengers of malondialdehyde in vitro and in vivo[J].Nanoscale Research Letters,2013,8:190.
[35]Zhang M H,Feng L,Gu J F,et al.The attenuation of Moutan Cortex on oxidative stress for renal injury in AGEs-induced mesangial cell dysfunction and streptozotocin-induced diabetic nephropathy rats[J].Oxidative medicine and cellular longevity,2014,2014:1-13.
[36]Dai M,Xie P,Liang G,et al.Simultaneous determination of microcystin-LR and its glutathione conjugate in fish tissues by liquid chromatography-tandem mass spectrometry[J].Journal of Chromatography B,2008,862(1/2):43-50.
[37]Liu X J,Luo Z,Xiong B X,et al.Effect of waterborne copper exposure on growth,hepatic enzymatic activities and histology in Synechogobius hasta[J].Ecotoxicology and Environmental Safety,2010,73(6):1286-1291.
[38]Thophon S,Kruatrachue M,Upatham E S,et al.Histopathological alterations of white seabass,Lates calcarifer,in acute and subchronic cadmium exposure[J].Environmental Pollution,2003,121(3):307-320.
[39]Lübcker N,Dabrowski J,Zengeya T A,et al.Trophic ecology and persistence of invasive silver carp Hypophthalmichthys molitrix in an oligotrophic South African impoundment[J].African Journal of Aquatic Science,2016,41(4):399-411.
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[2]Chen W,Jia Y L,Li E H,et al.Soil-based treatments of mechanically collected cyanobacterial blooms from Lake Taihu:Efficiencies and potential risks[J].Environmental Science&Technology,2012,46(24):13370-13376.
[3]Shang L X,Feng M H,Liu F F,et al.The establishment of preliminary safety threshold values for cyanobacteria based on periodic variations in different microcystin congeners in Lake Chaohu,China[J].Environmental Science:Processes&Impacts,2015,17(4):728-739.
[4]Li D H,Wang Z C,Qin H J,et al.An integrated technology of bloom-barrier and bloom-trap for cyanobacterial bloom control[J].Resources&Environment in the Yangtze Basin,2012,21(Z2):45-50.
[5]Qin H J,Zhang Z Y,Liu H Q,et al.Fenced cultivation of water hyacinth for cyanobacterial bloom control[J].Environmental Science and Pollution Research,2016,23(17):17742-17752.
[6]Li H B,Hou G X,Feng D K,et al.Prediction and elucidation of the population dynamics of Microcystis spp.in Lake Dianchi(China)by means of artificial neural networks[J].Ecological Informatics,2007,2:184-192.
[7]Feurstein D,Stemmer K,Kleinteich J,et al.Microcystin congenerand concentration-dependent induction of murine neuron apoptosis and neurite degeneration[J].Toxicological Sciences,2011,124(2):424-431.
[8]Campos A,Vasconcelos V.Molecular mechanisms of microcystin toxicity in animal cells[J].International Journal of Molecular Sciences,2010,11(1):268-287.
[9]Corbel S,Mougin C,Boua?cha N.Cyanobacterial toxins:Modes of actions,fate in aquatic and soil ecosystems,phytotoxicity and bioaccumulation in agricultural crops[J].Chemosphere,2014,96:1-15.
[10]张慧,姜锦林,张宇峰,等.微囊藻毒素-LR和铜绿微囊藻裂解液对营养生长期水稻生理生化效应[J].中国环境科学,2017,37(8):3134-3141.Zhang H,Jiang J L,Zhang Y F,et al.Physiological and bio-chemical effects of pure MC-LR and Microcystis aeruginosa crude extracts on Oryza sativa L.at vegetative stage[J].China Environmental Science,2017,37(8):3134-3141.
[11]时玥,姜锦林,邓正栋.微囊藻毒素-LR和铜绿微囊藻裂解液对水稻光合作用的影响[J].中国环境科学,2017,37(11):4284-4293.Shi Y,Jiang J L,Deng Z D.Effects of pure MC-LR and Microcystis aeruginosa crude extracts on photosynthesis of Oryza sativa L[J].China Environmental Science,2017,37(11):4284-4293.
[12]Saqrane S,ghazali I E,Ouahid Y,et al.Phytotoxic effects of cyanobacteria extract on the aquatic plant Lemna gibba:Microcystin accumulation,detoxication and oxidative stress induction[J].Aquatic Toxicology,2007,83(4):284-294.
[13]Kosiba J,KrztońW.Effect of microcystins on proto-and metazooplankton is more evident in artificial than in natural waterbodies wilk-wo?niak E[J].Microbial Ecology,2018,75(2):293-302.
[14]Sun H,LüK,Minter E J A,et al.Combined effects of ammonia and microcystin on survival,growth,antioxidant responses,and lipid peroxidation of bighead carp Hypophthalmythys nobilis larvae[J].Journal of Hazardous Materials,2012,221-222:213-219.
[15]Manach S L,Sotton B,Huet H,et al.Physiological effects caused by microcystin-producing and non-microcystin producing Microcystis aeruginosa on medaka fish:A proteomic and metabolomic study on liver[J].Environmental Pollution,2018,234:523-537.
[16]Stewart I,Seawright A A,Shaw G R.Cyanobacterial poisoning in livestock,wild mammals and birds-an overview.In Cyanobacterial harmful algal blooms:state of the science and research needs[M].New York:Springer,2008:613-637.
[17]Carmichael W W.Health effects of toxin-producing cyanobacteria:“the CyanoHABs”[J].Human and Ecological Risk Assessment,2001,7(5):1393-1407.
[18]Azevedo S M F O,Carmichael W W,Jochimsen E M,et al.Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil[J].Toxicology,2002,181:441-446.
[19]WHO.Toxic cyanobacteria in water:A guide to their public health consequences,monitoring and management[M].London:CRC Press,1999:60-62.
[20]Malbrouck C,Kestemont P.Effects of microcystins on fish[J].Environmental Toxicology and Chemistry,2006,25(1):72-86.
[21]Triest L,Stiers I,Onsem S V.Biomanipulation as a nature-based solution to reduce cyanobacterial blooms[J].Aquatic Ecology,2016,50(3):461-483.
[22]Guo L G,Wang Q,Xie P,et al.A non-classical biomanipulation experiment in Gonghu Bay of Lake Taihu:control of Microcystis blooms using silver and bighead carp[J].Aquaculture research,2015,46:2211-2224.
[23]Torres G S,Silva L H S,Rangel L M,et al.Cyanobacteria are controlled by omnivorous filter-feeding fish(Nile tilapia)in a tropical eutrophic reservoir[J].Hydrobiologia,2016,765(1):115-129.
[24]Lawton L A,Edwards C.Purification of microcystins[J].Journal of Chromatography A,2001,912(2):191-209.
[25]Harada K I,Suzuki M,Dahlem A M,et al.Improved method for purification of toxic peptides produced by cyanobacteria[J].Toxicon,1988,26:433-439.
[26]Li X Y,Chung I K,Kim J I,et al.Subchronic oral toxicity of microcystin in common carp(Cyprinus carpio L.)exposed to Microcystis under laboratory conditions[J].Toxicon,2004,44(8):821-827.
[27]Xie L Q,Xie P,Ozawa K,et al.Dynamics of microcystins-LR and-RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment[J].Environmental Pollution,2004,127(3):431-439.
[28]Shen Q,Hu J,Li D H,et al.Investigation on intake,accumulation and toxicity of microcystins to silver carp[J].Fresenius Environmental Bulletin,2005,15(12):1124-1128.
[29]Papadimitriou T,Kagalou I,Stalikas C,et al.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[J].Ecotoxicology,2012,21(4):1155-1166.
[30]Magalhaes V F,Soares R M,Azevedo S M.Microcystin contamination in fish from JacarepaguáLagoon(Rio de Janeiro,Brazil):ecological implication and human health risk[J].Toxicon,2001,39:1077-1085.
[31]Al-Ghais S M.Acetylcholinesterase,glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish[J].Marine Pollution Bulletin,2013,74(1)183-186.
[32]Wang Y C,Jiang L,Li Y F,et al.Excessive selenium supplementation induced oxidative stress and endoplasmic reticulum stress in Chicken Spleen[J].Biological Trace Element Research,2016,172(2):481-487.
[33]Bliss C I.Some principles of bioassay[J].American Scientist,1957,45(5):449-466.
[34]Deng Y,Wang W,Yu P F,et al.Comparison of taurine,GABA,Glu,and Asp as scavengers of malondialdehyde in vitro and in vivo[J].Nanoscale Research Letters,2013,8:190.
[35]Zhang M H,Feng L,Gu J F,et al.The attenuation of Moutan Cortex on oxidative stress for renal injury in AGEs-induced mesangial cell dysfunction and streptozotocin-induced diabetic nephropathy rats[J].Oxidative medicine and cellular longevity,2014,2014:1-13.
[36]Dai M,Xie P,Liang G,et al.Simultaneous determination of microcystin-LR and its glutathione conjugate in fish tissues by liquid chromatography-tandem mass spectrometry[J].Journal of Chromatography B,2008,862(1/2):43-50.
[37]Liu X J,Luo Z,Xiong B X,et al.Effect of waterborne copper exposure on growth,hepatic enzymatic activities and histology in Synechogobius hasta[J].Ecotoxicology and Environmental Safety,2010,73(6):1286-1291.
[38]Thophon S,Kruatrachue M,Upatham E S,et al.Histopathological alterations of white seabass,Lates calcarifer,in acute and subchronic cadmium exposure[J].Environmental Pollution,2003,121(3):307-320.
[39]Lübcker N,Dabrowski J,Zengeya T A,et al.Trophic ecology and persistence of invasive silver carp Hypophthalmichthys molitrix in an oligotrophic South African impoundment[J].African Journal of Aquatic Science,2016,41(4):399-411.
[40]Infante A,Riechl W.The effect of cyanophyta upon zooplankton in a eutrophic tropical lake(Lake Valencia,Venezuela),In Tropical Zooplankton[M].Dordrecht:Springer,1984:293-298.
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