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Dietary Selenium Reduces Retention of Methyl Mercury in Freshwater Fish Poul Bjerregaard,*,† Susanne Fjordside,† Maria G. Hansen,† and Maya B. Petrova† †
Institute of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark ABSTRACT: Adverse effects from organic mercury transported along aquatic food chains are health issues in humans and other top predators. Methyl mercury in organisms at the lower food chain levels is eliminated slowly, and laboratory studies have not clarified the role of selenium in the retention of methyl mercury in fish. Here, we investigated the effects of dietary selenium on the retention of organic and inorganic mercury in freshwater fish. Addition of selenite to the food augmented elimination of methyl mercury (but not inorganic mercury) from goldfish Carassius auratus in a dose dependent manner; selenite caused methyl mercury to be lost from the general body rather than from any specific organ. Seleno-cystine and seleno-methionine (but not selenate) likewise promoted elimination of methyl mercury from goldfish. The threshold for the augmenting effect of selenite on the elimination of methyl mercury in the zebra fish Danio rerio was 0.95 μg Se g 1 food; higher concentrations reduced retention of methyl mercury in a dose dependent manner. Selenium concentrations in the food approaching natural background levels increase the elimination of methyl mercury from fish. Thus, selenium levels in a given aquatic food chain may affect mercury contamination along the food chain.
’ INTRODUCTION Anthropogenic mobilization of mercury has caused an increase in the flux of mercury through the global atmosphere1 and subsequent elevation of methyl mercury concentrations in aquatic ecosystems also in remote areas far from direct discharges of mercury.2 Methyl mercury is readily assimilated from both food and water in most aquatic organisms, and once assimilated, methyl mercury is retained very efficiently, with biological half-lives in various aquatic organisms typically ranging from several weeks in daphnia3 to years in some fish e.g. pike Esox lucius4 and rainbow trout Oncorhynchus mykiss.5 The level of methyl mercury attained by predators at the top of aquatic food chains is generally determined by biomagnification processes up through the food chain, and the major amount of methyl mercury enters the aquatic food chains at the lower trophic levels.6 Hence the ability of the various species in the food chain to eliminate methyl mercury determines the levels of methyl mercury attained at the upper end of the food chain where methyl mercury may cause toxic effects in top predators among wildlife7 and neurological symptoms in children of women with a high fraction of aquatic organisms in their diet.8 Selenium interacts with the accumulation and toxicity of mercury in aquatic organisms in fairly complicated ways. In some marine mammals, demethylation of methyl mercury in the liver leads to formation of insoluble HgSe9 giving rise to a 1:1 molar ratio Hg:Se.10 Contrary to this, fish11 13 and crayfish11 in experimental lakes treated with selenium decreased their mercury contents, and fish in selenium contaminated areas have been shown to contain reduced amounts of mercury.14 16 r 2011 American Chemical Society
Laboratory investigations on the effect of selenium on mercury handling in fish and aquatic invertebrates have shown highly variable results (reviewed by17,18), apparently depending on the form of the elements (organic/inorganic), exposure routes (injection, water, food), and timing and concentration of the exposure and the organism in question. Therefore, the results of the previous laboratory investigations are not able to explain the recent finding19 that fish in streams of the Western part of USA show lower concentrations of methyl mercury in areas with high selenium levels. However, the fact that selenium administered in the food reduces the concentrations of methyl mercury in liver, kidney, and muscle of rainbow trout Oncorhynchus mykiss20 raises the question if dietary selenium generally affects the retention of methyl mercury in fish. Therefore, the purpose of the present investigation was to elucidate the effect of dietary selenium on mercury retention in fish; goldfish Carassius auratus and zebrafish Danio rerio were used as test organisms.
’ EXPERIMENTAL SECTION Experimental Animals. Commercially bred fish were used in the experiments. The size ranges were 4 to 8 cm (average 6.4 g) for the goldfish Carassius auratus and 0.5 to 1.0 g for the zebrafish Received: July 25, 2011 Accepted: October 20, 2011 Revised: September 28, 2011 Published: October 20, 2011 9793
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Environmental Science & Technology Danio rerio. The fish were acclimated to laboratory conditions for at least one week before experiments. Goldfish and zebrafish were chosen as experimental animals because of their experimental robustness and small enough sizes to fit into the gamma counters for live counting. Exposure to 203Hg. The fish received radioactively labeled mercury (203Hg) at activities of approximately 10.000 counts per minute (cpm), either by intraperitoneal injections (goldfish) or administered in the food (zebrafish). The goldfish were anesthetized in MS-222 (ethyl 3-aminobenzoate methenesulfonate salt; Sigma-Aldrich, Brøndby, Denmark) during injection, and the mercury was dissolved in 0.9% NaCl. Preparation of Food. For experiment 1, selenite enriched trout food was produced specially by Dansk Ørredfoder, Brande A/S. Chemical analysis showed the selenite enriched food to contain 4.7 ( 0.1 μg Se g 1 and the control food to contain 1.5 ( 0.1 μg Se g 1. For experiments 2 and 3, 9 g of commercially purchased food for goldfish (Vitakraft, Bremen) was homogenized in a blender together with 20 mL of water, and 2 g of gelatin (Fluka, BioChimika) was added. The mixture was heated until the gelatin dissolved, and the desired amount and form of selenium was added. The mixture was thoroughly mixed, poured on a glass plate, cooled, and cut into cubes of suitable sizes. For experiment 4, a similar procedure was used except soft parts of blue mussels (Mytilus chilensis) were homogenized instead of goldfish food and no water was added. The concentration of selenium in the food was determined. The Hg-containing food was prepared by the same procedure. Experimental Setups. In experiment 1, groups of 7 goldfish were kept in 40 L aquaria; different coloration allowed recognition of individual fish. In experiments 2 and 3, the fish were kept individually in 2 L aquaria. In experiment 4, the zebrafish were kept individually in 1 L aquaria. The goldfish were kept in tap water (groundwater) at 12.5 °C and the zebrafish at 26 °C in a mixture of 1/3 tap water (groundwater) and 2/3 deionized water, both with a 12:12 light:dark regime. The fish were fed between 1 and 2% of their body weight each day. Experimental Design. The fish received the 203Hg via injection or food where after they were fed control food for 1 to 7 days until feeding with selenium supplemented food began (day 0 of the experiment). The radioactivity of each individual fish was determined by live counting at day 0 and defined as 100%. The radioactivity of each fish was determined regularly and expressed as a percentage of the activity at day 0. Counts were corrected for the physical decay of 203Hg. Experiment 1. It was investigated if injected 203HgCl2 or CH3-203HgCl were retained differently in goldfish fed selenite amended (4.7 ( 0.1 μg Se g 1) or control (1.5 ( 0.1 μg Se g 1) food. Retention of methyl mercury and inorganic was recorded over 77 and 76 days, respectively. After the exposure the organs and a sample of dorsal muscle tissue were dissected out, and the level of 203Hg in the organs was determined. Experiment 2. The effect of the doses of selenium in the food (0, 11, 22, or 39 μg Se g 1) on the retention of injected CH3-203HgCl was studied. The retention of mercury was monitored over 31 days. Experiment 3. The effect of the form of selenium in the food on the retention of injected CH3-203HgCl was studied. The retention of mercury was registered over 28 days in goldfish fed 15 to 17 μg Se g 1 in the form of selenite, selenate, selenomethionine, or seleno-cystine. The control group received food containing 0.19 μg Se g 1.
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Figure 1. Carassius auratus. Retention of methyl mercury (A) and inorganic (B) mercury in whole body goldfish after intraperitoneal injection of radioactively labeled inorganic Hg or methyl-Hg. Mean ( SEM for 7 8 fish in each group. O and dotted lines: Control food (1.5 μg Se g 1). b and solid lines: Selenite amended food (4.7 μg Se g 1).
Experiment 4. The purpose was to identify the threshold for the concentration of selenite in the food capable of augmenting the elimination of methyl mercury in zebrafish. Thirty-six zebrafish were fed food (based on mussel homogenate) containing CH3-203HgCl for a couple of days until they reached activities between 5000 and 21,000 cpm. The fish were then fed control food (0.408 ( 0.004 μg Se g 1) for 2 days where after the fish were separated into 6 groups, and feeding with the selenite enriched food (0.408 ( 0.004 [control], 0.51 ( 0.15, 0.95 ( 0.29, 1.37 ( 0.24, 2.1 ( 0.7, and 5.6 ( 1.4 μg Se g 1) was initiated. Chemicals. Selenite was purchased from Merck, Darmstadt, sodium selenate from Bie and Berntsen A/S. Seleno-L-methionine and seleno-DL-cystine (the diselenide form of selenocysteine) were obtained from Sigma-Aldrich. 203HgCl2 was obtained from Risø, Denmark, and CH3-203HgCl was synthesized from 203HgCl2 according to ref 21. Chemical Analysis. The radioactivity of the live goldfish was determined in a 7.6 cm well-type Bicron NaI(Tl) crystal gamma counter. The radioactivity of tissues and of the live zebrafish was determined in a Wizard TM3 automatic gamma counter. Selenium concentrations in the food were determined by hydride generation as described in ref 22; PerkinElmer 2380 and FIAS 100 atomic absorption spectrophotometers were used in experiments 1 and 2 to 4, respectively. The reliability of the selenium analysis was investigated by including standard material (DORM and TORT); the measured values were within the certified range. Data Treatment. The activity of each fish was set to 100%, the day the selenium exposure began. Repeated measures ANOVA analysis was used to check for difference in elimination of mercury between the groups (significance level: α = 0.05). The retention of mercury was fitted to first (Ct = C0*e k/t) or second 9794
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Figure 3. Carassius auratus. Retention of organic mercury in goldfish fed different concentrations of selenite in the food. O: Control food (0.19 μg Se g 1). 9: 11 μg Se g 1. 2: 22 μg Se g 1. ): 39 μg Se g 1. Mean ( SEM for 5 or 6 fish in each group.
Figure 2. Carassius auratus. Distribution of methyl mercury (A) and inorganic mercury (B) after 11 weeks’ exposure to 1.5 (open bars) or 4.7 (solid bars) μg Se g 1 in the food. Mean ( SEM for 7 or 8 fish. * indicates that the difference between the two groups is statistically significant at the 0.05 level. Percent distribution calculated at the end of the experiment.
(Ct = A*e a/t + B*e b/t) order kinetics. The half-life for the most rapidly exchangeable pool of methyl mercury was estimated from the tangent to the elimination curve at day zero.
’ RESULTS In all of the experiments the fish consumed both control food and the selenium amended food without any signs of reluctance to eat or adverse effects. Retention of organic and inorganic mercury in goldfish could both be described by two compartment models. Eighty and 69% of the methylmercury and inorganic mercury, respectively, were retained in compartments with no discernible elimination (Figure 1); half-lives for methylmercury and inorganic mercury in the exchangeable compartments were 77 and 57 days, respectively. Exposure to selenite in the food augmented the elimination of methyl mercury from the exchangeable pool of methyl mercury (t1/2 = 37 days; Figure 1A), whereas there was no significant effect on the elimination of inorganic mercury (Figure 1B). Seventy-six to 77 days after the injection of the radioactively labeled mercury, the methyl mercury was bound especially in muscle and residual tissues (Figure 2A), whereas the inorganic mercury was bound predominantly in liver, gut, kidney, and residual tissues (Figure 2B). Exposure to selenite in the food did not lead to any redistribution among the tissues of the methyl mercury retained in the goldfish, so the selenium induced increase in the elimination of methyl mercury could not be attributed to augmented loss from any particular tissue or organ. The liver of the selenite exposed goldfish contained a significantly lower percentage of the body burden of inorganic mercury than the livers of the nonexposed group (Figure 2B).
Figure 4. Carassius auratus. Retention of organic mercury in goldfish fed different forms of selenium in the food. O: Control food (0.19 μg Se g 1). 2: Selenate (16 μg Se g 1). 9: Seleno-methionine (16 μg Se g 1). (: Seleno-cystine (15 μg Se g 1). b: Selenite (16 μg Se g 1). Mean ( SEM for 5 or 6 fish in each group.
Exposure to 11 and 22 μg Se g 1 in the food caused a dosedependent increase in the elimination of methyl mercury from the goldfish, whereas exposure to 39 μg Se g 1 in the food caused no further increase in the elimination rate than exposure to 22 μg Se g 1 (Figure 3). Exposure to selenium in the form of selenite, seleno-cystine, and seleno-methionine in the food all increased the elimination rate for methyl mercury, while the elimination rate in the group exposed to selenate did not differ from the elimination rate in the control group (Figure 4). In zebrafish Danio rerio, administration of food with selenium concentrations between 0.95 and 5.6 μg Se g 1 caused a dose dependent decrease in the retention of methyl mercury; there was a trend that the group fed food with selenium concentrations at 0.51 μg Se g 1 eliminated methyl mercury faster than the 9795
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Figure 5. Danio rerio. Retention of organic mercury in zebrafish fed different concentrations of selenite in the food. O: Control food (0.41 μg Se g 1). 2: 0.51 μg Se g 1. 9: 0.95 μg Se g 1. (: 1.37 μg Se g 1. b: 2.1 μg Se g 1. 1: 5.6 μg Se g 1. Mean ( SEM for 5 or 6 fish in each group (except the group exposed to 5.6 μg Se g 1, where n = 3).
control group (0.41 μg Se g ), but the difference was not statistically significant (Figure 5). Amendment of the food with selenite decreased the half-lives for methyl mercury in both goldfish (Figure 6A) and zebrafish (Figure 6B), but the effect of small increases relative to the background selenium concentrations in the food appeared more pronounced in the zebrafish than in the goldfish. 1
’ DISCUSSION Exposure to selenium in the food reduces retention of methyl mercury, but not inorganic mercury, in fish. Methyl mercury appears to be lost from the entire organism, rather than from any specific tissue or organ. Mercury concentrations in fish have generally been shown to be reduced in freshwater environments contaminated with selenium or in experimental lakes where selenium concentrations have been modified. Addition of selenite to controlled field enclosures reduced mercury accumulation in pike Esox lucius,23 pearl dace Semotilus margarita, yellow perch Perca flavescens, and white sucker Catostomus commersoni11 and addition of selenite to experimental lakes in Sweden reduced the concentrations of mercury in perch Perca fluviatalis, roach Leuciscus rutilus, and pike E. lucius.12,13 Mercury concentrations in largemouth bass Micropterus salmoides increased in a quarry from which fly ash discharges high in selenium were eliminated,14 and mercury concentrations in freshwater organisms generally decreased with increasing selenium concentrations in a selenium contaminated area.16 Based on the inverse relationship between the contents of selenium and mercury in perch Perca flavescens and walleye (Stizosedion vitreum), Chen et al.24 suggested that exposure to selenium reduces the assimilation of mercury in fish. These field observations are, however, not readily explained by the knowledge on selenium mercury interactions obtained from laboratory experiments, since studies on the effect of selenium on mercury handling in fish show highly variable results, depending on the form of the two elements, the exposure routes, and the timing and doses/concentrations of the exposures. When injected
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Figure 6. Carassius auratus and Danio rerio. Relations between half-lives for methyl mercury and selenium concentrations in the food amended with selenite. ): Exp. 1; 1: Exp. 2; 2: Exp. 3; 0: Exp. 4.
intramuscularly, selenite (0.4 mg Se kg 1) did not affect the overall body retention of injected methyl mercury (1 mg Hg kg 1) in killifish Fundulus heteroclitus over 24 h, but the selenite exposure led to a redistribution of methyl mercury among the organs resulting in decreased concentrations in kidney and red blood cells.25 Exposure to 2.5 and 5 mg Se kg 1 wet wt food (as selenite) did not affect accumulation from food (2.5 mg Hg kg 1 wet wt) of methyl mercury in muscle and liver of cod Gadus morhua over 32 days, whereas selenite exposure increased methyl mercury accumulation in the brain.26 Exposure to selenite and selenate in the water (2 and 200 μg Se L 1) did not affect the accumulation of methyl mercury from water (1 μg Hg L 1) in tissues of plaice Pleuronectes platessa.27 Exposure of zebrafish larvae to selenomethionine ameliorated some of the neurobehavioral effects of concurrent exposure to methyl mercury but had no effect on the accumulation of mercury.28 Waterborne selenite did not affect methyl mercury accumulation in zebrafish Brachydanio rerio29 and medaka Oryzias latipes.30 Exposure to 9.7 μg Se-SeO3— g 1 in the food reduced the concentrations of methyl mercury in liver, kidney, and muscle in rainbow trout.20 Concerning the effects of selenium on the kinetics of inorganic mercury, it is also difficult to obtain a clear picture from the experiments carried out with fish.27,31 34 In the majority of the investigations mentioned above, aspects of mercury uptake and accumulation processes were studied, whereas only the retention of accumulated mercury is considered in the present investigation. The results of the present investigation may indicate that in the in situ investigations in which selenium has been shown to lower the mercury concentrations in fish,11 13,15,16,23,24 selenium has affected elimination rather than uptake processes. Selenium concentrations in freshwater fish generally increase with the concentration of selenium in the water24 although direct uptake from the water phase may differ among species. Rainbow trout readily accumulates selenium in the tissues upon exposure 9796
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Environmental Science & Technology to waterborne selenite,35 whereas turbot Scophthalmus maximus accumulates selenium in the tissues from selenite in the water very slowly or not at all.36 Although rainbow trout is able to accumulate selenium directly from water, food is considered to be the dominant source of selenium37,38 as it is indeed in many aquatic organisms.39,40 Furthermore,41 it is suggested that dietary selenium is metabolized in the liver of trout and stored in organic form, while selenite taken up from water is stored as inorganic selenium. It is thus conceivable that selenite given in the water phase may affect mercury handling differently from dietary selenite, both in terms of the amount and the chemical form of selenium present in the tissues for interaction with mercury. Administration of selenate does not appear to affect the retention of methyl mercury in goldfish, and this is in accordance with the knowledge that selenate is taken up very slowly or not at all in aquatic organisms.22 The biochemical mechanisms underlying the effects of selenium on the elimination of mercury from fish observed in the present laboratory study and in situ investigations11 13,23 are not known. Since the laboratory studies on the effect of selenium on mercury retention indicate that selenium administered in the food is the only route of administration that has consistent effects on methyl mercury retention, interactions between selenium and mercury within the digestive tract may be hypothesized. Entero-hepatic recirculation of methyl mercury in rainbow trout 42 has been suggested to explain the long half-life (>200 days) for methyl mercury observed,5,43 and it is possible that selenite in the food could react (e.g., microbiologically) in the intestine to form compounds that could bind methyl mercury and thus interrupt the entero-hepatic recirculation, leading to elimination of the methyl mercury via the faeces. In some organisms, selenium present in the tissues is known to ameliorate the toxic effects of accumulated methyl mercury by interactions at the molecular level.44 46 This has generated interest in elucidating molecular ratios between selenium and mercury in tissues with the aim of identifying the amount of selenium needed to be present to protect against the adverse effects of methyl mercury. In a recent investigation on the mercury and selenium concentrations in streams of the western USA, Peterson et al.19 concluded that ‘high Hg concentrations in fish tissue.... were found only when Se concentrations in the same tissue were low’. The results of the present investigation underline the need to consider the effect of selenium on methyl mercury biokinetics as well as the interactions at the biochemical level in the tissues if the full mechanism underlying selenium’s influence on mercury biomagnification and toxicity is to be elucidated.
’ AUTHOR INFORMATION Corresponding Author
*Phone: +45 6552456. Fax: 45 6550 2786. E-mail: poul@ biology.sdu.dk.
’ ACKNOWLEDGMENT We thank Dansk Ørredfoder A/S, Brande, Denmark, for supplying the selenite amended food used in experiment 1. This investigation was supported by grants from the Danish Natural Science Research Council. ’ REFERENCES (1) UNEP. Global Mercury Assessment; United Nations Environment Programme Chemicals: Geneva, Switzerland, 2002; pp 1 270.
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