ISSN 19950829, Inland Water Biology, 2013, Vol. 6, No. 2, pp. 155–160. © Pleiades Publishing, Ltd., 2013. Original Russian Text © A.A. Filippov, I.L. Golovanova, A.I. Aminov, 2013, published in Biologiya Vnutrennikh Vod, 2013, No. 2, pp. 78–84.
AQUATIC TOXICOLOGY
Effects of Organic Pollutants on Fish Digestive Enzymes: A Review A. A. Filippov, I. L. Golovanova, and A. I. Aminov Papanin Institute of the Biology of Inland Waters, Russian Academy of Sciences, Borok, 152742 Russia email:
[email protected] Received November 22, 2011
Abstract—A brief overview of data on the effects of organic pollutants of different chemical natures (orga nochlorine, organophosphorous and organotin compounds, naphthalene, formalin, nitrosoguanidine, gly phosate, and metylmercury) on the activity of fish enzymes hydrolyzing basic food components is given. It is shown that the xenobiotics listed above have different effects on fish digestive enzymes. The directions of tox icantinduced changes may differ depending on the fish species, type of hydrolyzed substratum, diapason of toxicant concentrations, and experimental conditions. Keywords: organic pollutants, fishes, digestive enzymes DOI: 10.1134/S199508291302003X
Organic pollutants are considered particularly dan gerous toxicants. They are widespread in the environ ment and most of them are resistant to the effects of physical and chemical agents and are weakly degradable under natural conditions [24]. Owing to the lack of complete data on bioaccumulation and the longterm effects of these compounds on living beings, no com monly accepted list of these toxicants exists. However, according to the protocol of the 2001 Stockholm Con ference, 12 persistent organic pollutants (POPs) were classified as extremely dangerous and demanding urgent measures aimed in their deactivation. Entering an organism with water, food [36–38], and bottom sediments [30], organic pollutants may accumulate in various tissues and organs, changing development, growth, and reproduction in fish [23, 31, 49–51]. Even at very low doses they exhibit toxic, mutagenic, and carcinogenic effects [3, 15, 28, 43]; change fish behavior [32, 44]; impair the hormonal balance [34] and metabolism of vitamins and mineral elements [16]; and cause various morphological pathologies [27, 42]. Fish are most sensitive to the effects of organic pollutants at early developmental stages [51, 53]. The changes in the rates of metabolism in the developing embryos and larvae affected by pes ticides may be determined by the impairment of the processes of energy generation and use [45]. The intestine plays an important role in the absorp tion and metabolism of many organic pollutants [41, 52, 56]. Disorders of several morphofunctional characteristics of the fish digestive tract were noted upon exposure to xenobiotics [7, 11, 12, 28, 29, 39, 47, 48, 55]. For instance, the alimentary uptake of polycy clic aromatic hydrocarbon (PAH) benzo[a]pyrene at a dose of 20 mg/kg in European seabass (Dicentrarchus labrax (L.) and at a dose of 12.5 μg/kg in orangespot
ted grouper (Epinephelus coioides (Hamilton) caused ultrastructural alterations in the cells of intestine epi thelium: hyperplasia of enterocytes, the destruction of intercellular contacts and mitochondria, increased cellular proliferation, and the formation of crypts [41, 56]. The exposure of Nile tilapia (Oreochromis niloticus (L.) for 24 h to the waterborne pyrethroid insecticide neobiputrin at a concentration of 1/2 LC50 resulted in changes in the structure and decreases in the number of dense contact of the intestinal epithelial cells, indicating a decrease in the content of membrane proteins (including enzymes) and in the permeability of the intestinal mucosa [46]. A decrease in the intestinal transport of glucose was reported in spotted snakehead Channa punctatus (Bloch) exposed to endosulfan and chinalphos pesticides for 96 h at LC50 [48]. Organic pollutants of various natures may change the activities of the enzymes hydrolyzing the main components of food in the fish digestive tract [1, 6–9, 11, 20, 21, 33, 35, 36, 40]. Chronic experiments revealed that polychlorinated biphenils ((PCBs) belonging to the class of organochlorine polycyclic aromatic compounds) in food (50.8 ng/g wet weight) and in bottom sediments (426 ng/g dry weight) decrease the rates of the initial stages of assimilation of carbohydrates and proteins in the intestine of roach (Rutilus rutilus (L.)) underyearlings [9]. The activity of glycosidases in the intestine mucosa decreased by 11– 33% in 96 days, while the values of the Michaelis con stant (Km) of starch hydrolysis increased by 23% by the 218th day, indicating a decrease in the affinity of the enzyme to the substrate. The activities of proteinases in the underyearlings of the exposed group decreased by 11–26% by 40th, 96th, and 218th days of exposure. The increase in the ratio of amylolytic : proteolytic activities in the roach underyearlings suggests a higher
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sensitivity of roach proteinases to the chronic effect of PCBs when compared to glycosidases. The activities of enzymes in the gut content (chyme) in juvenile roach chronically exposed to PCBs changed in differ ent directions depending on the duration of the exper iment [9]. In addition, the increase in the PCB con centration in food and bottom sediments increased the sensitivity of glycosidases in the intestinal mucosa of roach underyearlings to the effects of Cu2+ and Zn2+ (0.1–25 mg/L) in vitro. Increased sensitivity occurs both owing to the inhibitory effect at the same concen tration and to the decline in the amylolytic activity at lower metal concentrations [33]. The study on the activity of glycosidases (αamy lase, sucrase, maltase, and amylolytic activity) in the intestine of bream (Abramis brama (L.)) of the Rybinsk Reservoir revealed that the activities of mal tase and enzyme affinity to the substrate were lower in the fish caught in the most polluted Sheksna Reach and having a higher liver PCB burden than in fish from the less polluted Mologa Reach [5]. At the same time, the activities of proteinases hydrolyzing protein com ponents of the food were 1.5 times higher in the bream from the Sheksna Reach than from the Mologa Reach [25]. Such differences may be determined by the higher content of protein in the tissues of fish preys inhabiting polluted habitats and by different effects of the toxicant on the proteolytic and glycolytic enzymes. Curves describing the temperature dependence in the bream from different habitats are quite close to each other (the thermal optimum of proteinases is 60°С; that of glycosidases is 50°С). However, in the bream from the Sheksna Reach within the vitality diapason, the values of the activation energy (Eact) of proteinases and glycosidases were higher, indicating a decrease in the efficiency of the hydrolysis of the main compo nents of food in the fish with higher PCB body burdens [13, 25]. At the same time, a significant decline in Km of hydrolysis of di and polysaccharides indicates an adap tive increase in the enzymesubstrate affinity along with an increase in the fishliver PCB content [5]. The chronic 60daylong exposure of Mozambique tilapia (Oreochromis mossambicus Peters) to naphtha lene (PAH) at a concentration of 1.5 mg/L (1/15 LC50 for 24 h) in fact did not change the amylolytic and pro teolytic activities in the fishintestine mucosa [35, 40]. The activities of these enzymes in the gut content may increase by 50–98% of the control. The experiments in vitro revealed that naphthalene at concentrations of 0.3–15 mg/L did not result in significant changes in amylolytic activity in 12 species of freshwater teleosts [35]. These results show that this PAH did not affect either the functioning of the membrane enzymes of the tilapia intestine or the processes of their synthesis. The shortterm exposure of fertilized fish eggs to chlorophos (organophosphorous pesticide) at con centrations of 1 × 10–6 to 1 × 10–2 mg/L provoked remote multidirectional effects that were manifested in changes on the activity and kinetic characteristics of
glycosidases in the intestine of developing juvenile roach [11]. The amylolytic activity in the intestinal mucosa of 4monthold underyearlings decreased when compared to the control fish. The maximal inhi bition by 45–49% was noted at the chlorophos con centrations of 1 × 10–5 and 1 × 10–4 mg/L. On the other hand, the activity of sucrase increased and the most pronounced stimulating effect (by 90–103%) was noted at the extreme points of the studied diapason of concentrations. Multidirectional effects of chlorophos during embryogenesis upon the amylolytic activity and activity of sucrase in roach underyearlings may be related to the different impact of toxicants on the syn thesis of pancreatic (αamylase) and specifically intes tinal (maltase and sucrase) enzymes. In the exposed fish, the values of Km of starch hydrolysis were 1.3– 3.8 times lower, reflecting the adaptive increases in the affinity of enzymes to substrate. In contrary, the values of Km of sucrase hydrolysis were increasing by two to four times inversely to the chlorophos concentration, indicating a decrease in the enzymesubstrate affinity and rate of disaccharides hydrolysis [11]. Toxic properties of chlorophos are determined mainly by its more toxic derivative, dimethyl divinil phosphate (DDVP). The experiments with Mozam bique tilapia have shown the chronic 60daylong exposure of fish to DDVP at a sublethal concentration of 0.46 mg/L (1/15 LC50 for 24 h) reversibly decreases gut amylolytic activity by ≤20% of the control but does not change proteolytic activity [35, 40]. In the experi ments in vitro, DDVP at concentrations of 0.2– 100 mg/L does not affect the activity of glycosidases in the intestine mucosa of 11 fish species inhabiting the Rybinsk Reservoir [36]. A significant decrease in the activity of proteinases by 21% of the control was noted only in pike upon the effect of DDVP at concentration of 0.2 mg/L. The comparison of DDVP effects in vivo and in vitro indicates that revealed changes in the enzymatic activity are nonspecific and the negative effect of chronic exposure to this toxicant is deter mined by its impact upon fishforaging behavior [44]. The shortterm exposure of fish during embryo genesis to NmethylN'nitroNnitrosoguanidine (MNNG), a genotoxic compound directly affecting the chemical structure of DNA, at a concentration of 7.5 mg/L changes the rate of hydrolysis of carbohy drates in the intestine of developing roach underyear lings and the sensitivity of digestive hydrolases to the impact of heavymetal salts [17]. Exposure to low con centrations (3 × 10–7–3 × 10–2) mg/L) of MNNG dur ing early embryogenesis decreases amylolytic activity and the activity of sucrase in the roach intestinal mucosa [12]. Upon extreme concentrations of the studied diapason, MNNG had similar effects: the amylolytic activity decreased by 30–41%; sucrase activity decreased by 31–46% of the control. The Km values of starch hydrolysis in the exposed underyear lings were 1.6–2.5 times lower than in the control; a maximal decrease of 58–60% was noted at the INLAND WATER BIOLOGY
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extreme values of the tested MNNG concentration diapason. The MNNG concentrationdependent changes in Km values of sucrose are of an oscillating character: the lowest values were noted upon toxicant concentrations of 3 × 10–5 mg/L and 3 × 10–1 mg/L [12]. As in the case with chlorophos, within the range of studied concentrations, MNNG induced multidi rectional changes in the sensitivity of digestive glycosi dases to the impact of copper and zinc ions in vitro in developing roach underyearlings. The magnitude and direction of the effects depend in the natures and con centrations of the interacting toxic agents [33]. The shortterm exposure of roach embryos to 0.0018% formalin (an aqueous solution of formalde hyde belonging to the aliphatic compounds) in most cases did not result in differences in the activities of proteinases and alkaline phosphatase between exposed and control juvenile roach [21]. However, a study on the thermal characteristics of alkaline phosphatase revealed a sharp narrowing of the zone of optimal val ues and a decrease in the thermal optimum (from 50 to 40°С) in the underyearlings that developed from eggs exposed to formalin [21]. The in vivo effects of two organotin compounds, triamyltin chloride (TATC) and triethyltin chloride (TETC) at concentrations of 0.5 mg/L and 1 mg/L, upon the activity of digestive enzymes in the common carp (Cyprinus carpio (L.), were studied [1, 2]. The study revealed that 1 to 3weeklong exposure to TATC did not affect the αamylase activity. TETC at the same concentrations suppressed the activities of αamylase, tripsin, and lipase 2–15 times when com paring to the control by first to second days of exposure [1, 2]. After exposure for 30 days at a lower concentra tion (0.01 mg/L and 0.001 mg/L), TATC induced a twofold irreversible decrease in the amylolytic activity, while TETC at concentrations of 0.01 mg/L and 0.003 mg/L induced multidirectional changes in the activities of the studied enzymes over 2 months of exposure. The regulatory mechanisms counteracting malfunction induced by nonspecific compounds facilitated the survival of exposed fish at unfavorable conditions [1, 2]. Methylmercury possessing lipophylic properties and easily penetrating the biological membranes is the most toxic organic compound. The accumulation of methylmercury in perch (Perca fluviatilis L.) from waterbodies with neutral water pH induces a nonspe cific decrease in the activities of digestive glycosidases and in the affinity of enzymes to substrate, which pre sumably partially compensates for the unfavorable influence of environmental factors on the rate of digestion of the carbohydrates in food [6]. The exper imental study of the effect of methylmercury in the natural food upon the activities of glycosidases and proteinases in the intestine mucosa of juvenile perch (duration of exposure 30 days) and silver crucian carp (Carassius auratus L.) (75 days) fed with food with low (0.11 mg/kg) and high (0.5 mg/kg) concentrations of mercury did not reveal changes in enzymatic activities INLAND WATER BIOLOGY
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[8]. However, longer exposure (3 months) of carp to higher concentrations of alimentary mercury inhibited the activity of glycosidases and the affinity of enzymes to substrate while the activity of proteinases increased [8]. The activity of pancreatic αamylase was sup pressed to a higher extent than the amylolytic or sucrase activities, indicating that the enzymes respon sible for the initial stages of hydrolysis of carbohy drates and functioning in the gut cavity are more sen sitive to the toxic effects of methylmercury compared to the specifically membrane enzymes [4]. A more detailed analysis of the impact of alimentary mercury revealed a decrease in the proteolytic activity in the intestine mucosa by 23.5–27% during first 2 months of the experiment [20]. From the third to fifth months, the differences in the studied parameters between exposed and control fish disappeared. After 6 months, the proteolytic activity was 27% higher than in the control. After 1 month of the experiment, the amy lolytic activity of the carp intestine was 10% higher; after 2 and 4 months, it was 13% and 11% lower than in the control, respectively [20]. The exposure of 4monthold roach to alimentary mercury (0.3– 0.4 mg/kg of food) decreased the activity of glycosi dases (sucrase and amylolytic activity) by 10–43% of the control and decreased the affinity of enzymes to substrate by 1.5–3 times, retarding the rate of carbo hydrates hydrolysis [7]. The presence of methymer cury in food at concentrations really present in the prey organisms may modify the activity of digestive hydrolases. Both inhibiting and stimulating effects are possible. It is worth noting that, in the in vivo experiments on the effects of methylmercury, chlorophos, and nitrozoguanidin, the decrease in the activity of gly cosidases responsible for the initial stages of carbohy drate hydrolysis was accompanied by an increase in fish length and weight. It is possible that the accelera tion of growth in juvenile fish upon the impact of sub lethal toxicant concentrations is determined by the compensatory increase in the efficiency of assimila tion of the protein components of food when com pared to carbohydrates. In addition, the low rate of the initial stages of carbohydrate assimilation may be compensated for by either a higher efficiency of the terminal stages of their assimilation or by a decrease in the energetic expenditures of the organism for loco motor activity, phenomenon that is often observed upon a high abundance of food under the conditions of toxic impact [3]. Upon chronic exposure of Asian silver carp Hypophtalmichthys molitrix Val., grass carp Ctenophar ingodon idella Val., common carp, and silver crucian carp to crude oil (10 mg/L and 100 mg/L), a decrease in the activities of αamylase, maltase, and casein lytic proteinases were noted [18]. By the sevenths day of exposure, the activities of all studied enzymes decreased at both concentrations of oil. After 14 days at a concentration of 10 mg/L, the trend toward the recovery of αamylase was noted; at a concentration of
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100 mg/L, the further suppression of glycosidases activity was observed. The activity of caseinlytic enzymes, on the other hand, recovered. The enzymes of silver and grass carps demonstrated the highest tol erance to oil intoxication [18]. The exposure of silver crucian carp in water containing bluegreen algae Microcystis sp. at concentrations of 1 × 107–3 × 104 cells/ml resulted in the accumulation of microcys tin (ring aldehyde), a cyanobacterial toxin, in the fish organism with the consequent growthrate retardation and suppression of the protease and amylase activities in the fish intestine and hepatopancreas [54]. The in vivo effects of the herbicide Roundup at concentrations of 0.1–50 mg/L (as per glyphosate) upon the activities of the enzymes (amylolytic activity and activity of sucrase) hydrolyzing the carbohydrates were studied in the intestine and whole organism of the juvenile tyulka fish (Clupeonella cultriventris (Nord.), pike (Esox lucius L.), roach, common carp, and perch [14]. The study revealed that the glycosi dases of the intestinal mucosa are more sensitive to toxic effects than similar enzymes in chyme and the whole organism [14]. Roundup has a more pro nounced toxic effect on the activities of glycosidases in the tissues of the real prey (the roach removed from the pike stomach) compared to similar enzymes of the potential prey. The magnitude and direction of the effects depend on the concentration of the toxi cant and spectrum of the enzymes participating in the hydrolysis of carbohydrates [5]. The enzymes of the preys may participate in fish digestion [19]. This is why the data on the effects of toxicants on the activity of hydrolases in the whole organisms of invertebrates and juvenile fish are of con siderable interest for trofology and fisheries practice. The exposure of the samples of crustacean plankton (including the representatives of the orders Cladocera, Copepoda, and Ostracoda) and of laboratory monoc ulture of Daphnia magna Straus. to Roundup (0.1 to 10.0 mg/L as glyphosate) in vitro did not reveal statis tically significant changes in the activities of glycosi dases [10]. Only at a concentration of 0.1 mg/L did Roundup induce an increase in amylolytic activity by 13% of the control in the samples of crustacean plank ton; at concentrations of 25.0 mg/L and 50.0 mg/L, it was 24% and 30%, respectively. In daphnia the sucrase activity increased by 28% and 85% of the control [10]. In chronic 15daylong tests, the Roundup solutions at sublethal concentrations of 25 mg/L and 50 mg/L (as per glyphosate) decreased the amylolytic activity by increasing the proteolytic activity in the tissues of daph nia of four generations [22]. Multidirectional changes in the activities of gly cosidases and proteinases were revealed in the whole organisms of daphnia and larvae of chironomid Chi ronomus riparius Meigen exposed to methylmercury in vivo [8]. Upon the separate exposure of these spe cies to methylmercury for one month, the amylolytic activity in the whole organism of daphnia decreased by 60% of the control; in the chironomids it did not
change. The activity of proteinases in daphnia did not change, while in chironomids it decreased to 60% of the control. When the invertebrates were exposed together in the same aquaria, the amylolytic and pro teolytic activities in daphnia did not change; in chi ronomids, it decreased by 30% and 69%, respectively. In the presence of methylmercury, the activity of sucrase in the tissues of the studied invertebrates was considerably higher than that in the control: 45% higher in daphnia and 53% higher in chironomids. The data given above indicate both the multidirec tional impact of mercury on the enzymes of carbohy drase and protease chains in the same species and the dependence of the magnitude and direction of the effect on the species of animal and experimental con ditions [8]. The data reviewed in the present paper show that the activity of digestive enzymes may be used as a physiological index of toxicity in the chronic experi ments and tests in vitro. The control of an experiment should be used as a norm of the physiological parame ter. The determination of thermal and kinetic charac teristics of the enzymes allow for revealing the mecha nisms of the response of a digestive system to the impact of xenobiotics. The given data conform well to the concept according to which toxicants (including organic compounds) within the known diapason of concentrations may not only suppress but also stimu late important vital functions of aquatic animals [26]. Chronic effects of the potentially toxic compounds on aquatic organisms are characterized by alternating periods of stimulation and suppression of the vitality indices at levels of both individuals and populations. A similar phase character also concerns the dependence of the effects of various concentrations of toxicants on digestive enzymes. The data on the effects of organic pollutants on the activities of enzymes hydrolyzing the main components of food may be used to forecast the risks of low amounts of organic toxicants on the effi ciency of digestion and the physiological–biochemi cal state of fish. REFERENCES 1. Buzinova, N.S., The effect of triethyl tin chloride on the digestive system of carp, in Olovoorganicheskie soedineniya i zhiznennye protsessy gidrobiontov (Organ otin Compounds and Life Processes of Aquatic Organ isms), Moscow: Mosk. Gos. Univ., 1975, pp. 209–215. 2. Buzinova, N.S., Pathological changes in the activity of digestive enzymes of fish, in Teoreticheskie problemy vodnoi toksikologii. Norma i patologiya (Theoretical Problems of Aquatic Toxicology: Normalcy and Pathology), Moscow: Nauka, 1983, pp. 131–137. 3. Glubokov, A.P., Growth of three species of fish in the early periods of ontogeny in normal state and under toxic exposure, Vopr. Ikhtiol., 1990, vol. 39, no. 1, pp. 137–143. 4. Golovanova, I.L., The influence of natural and anthro pogenic factors on the hydrolysis of carbohydrates in INLAND WATER BIOLOGY
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Translated by D. Pavlov INLAND WATER BIOLOGY
Vol. 6
No. 2
2013
