Influence of Eutrophication on Metal Bioaccumulation and Oral ...

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Influence of Eutrophication on Metal Bioaccumulation and Oral Bioavailability in Oysters, Crassostrea angulata Shun-Xing Li,*,†,‡ Li-Hui Chen,†,§ Feng-Ying Zheng,†,‡ and Xu-Guang Huang†,‡ †

College of Chemistry and Environment and ‡Fujian Province Key Laboratory of Modern Analytical Science and Separation Technology, Minnan Normal University, Zhangzhou 363000, China § Department of Food and Biological Engineering, Zhangzhou Institute of Technology, Zhangzhou 363000, China ABSTRACT: Oysters (Crassostrea angulata) are often exposed to eutrophication. However, how these exposures influence metal bioaccumulation and oral bioavailability (OBA) in oysters is unknown. After a four month field experimental cultivation, bioaccumulation factors (BAF) of metals (Fe, Cu, As, Cd, and Pb) from seawater to oysters and metal oral bioavailability in oysters by bionic gastrointestinal tract were determined. A positive effect of macronutrient (nitrate N and total P) concentration in seawater on BAF of Cd in oysters was observed, but such an effect was not significant for Fe, Cu, Pb, and As. Only OBA of As was significantly positively correlated to N and P contents. For Fe, OBA was negatively correlated with N. The regular variation of the OBA of Fe and As may be due to the effect of eutrophication on the synthesis of metal granules and heat-stable protein in oysters, respectively. KEYWORDS: eutrophication, metal oral bioavailability, metal bioaccumulation, oyster, food safety

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in oysters were evaluated by bionic gastrointestinal tracts.15 As similar as the biomembrane between the gastrointestinal tract and blood vessels, the liposome was used as the gastrointestinal absorption model. In vitro gastrointestinal digestion and gut metabolism were used for the pretreatment of oysters. Metal OBA was assessed by the ratio of affinity-liposome metal content in the chyme to total metal concentration in the oyster. In this article, we focused on the change of trophic status (i.e., N and P concentration) and evaluated its impact on bioaccumulation and oral bioavailability of metals in oysters by field experience.

INTRODUCTION Human inputs of nutrients to coastal waters can lead to the excessive production of algae, and this process was known as eutrophication.1 Most previous studies have demonstrated the close relationship between trophic status (N and P) and metal uptake in marine phytoplankton,2−5 but there have been few studies on marine bivalves, especially oysters. As a bivalve species, the oyster is sensitive to marine conditions, which has been used in the biomonitoring of coastal contamination,6,7 but few studies were focused on the effect of trophic status on the oyster’s metal bioaccumulation and oral bioavailability. The oyster, Crassostrea angulata, as a widespread seafood, is extensively cultivated in the coastal waters of South China, France, Portugal, and Spain.8,9 Oysters are an excellent source of Cu, Fe, and other nutrients. However, toxic metals (such as Cd) are also hyper-accumulated in oysters. Metal bioaccumulation and oral bioavailability in oysters are important for the consumers. Trace metal bioaccumulation in oysters is in response to some physicochemical properties such as temperature,10 salinity,11 and organic ligands compounds12 indicating that metal speciation could be transformed indirectly.13,14 Excessive uptake of metals could pose a danger to human health. Hence, the concentration and speciation of trace metal, especially As, Cd, and Pb, in oysters are very important for consumers. In the study, we first investigated whether there were any links between coastal eutrophication and metal bioaccumulation (or oral bioavailability, OBA) in oysters, which could shed light on the potential relationship between entrophication and metal bioaccumulation (or metal bioavailability for humans) in oysters. Metal bioaccumulation factor (BAF) was estimated by proportion of the oysters’ and water’s mass concentration. Only metal bioaccumulation in oysters cannot fully reflect the potential harm and nutrition from the consumption of oysters by humans. Therefore, metal speciation and oral bioavailability © 2014 American Chemical Society

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MATERIALS AND METHODS

Field Experiment and Sample Treatment. The oysters (crassostrea angulata) were collected from four semiclosed bays in Zhangzhou City, Fujian province, China with different trophic status: Fotan (FT: 24.20°N, 117.96°E), Jiuzhen (JZ: 24.01°N, 117.73°E), Gangwei (GW: 24.37°N, 118.09°E), and Zhao’an (ZA: 23.74°N, 117.32°E). According to the database from the Department of Ocean and Fisheries in Zhangzhou City, Fujian Province, China, four semiclosed bays were chosen. Among the bays, the trophic statuses were different, but the pH value, temperature, and metal concentration were similar. Monitoring of trophic status in these bays was done in the field every month to confirm these data from the database. Water samples (n = 3) were taken to analyze for total phosphorus (P) and nitrate (N), and the determination of N and P' concentration in seawater was based on the Chinese national standards GB/T 12763.42007 and GB11893-89, respectively. The salinities and pH value of seawater in Fotan (FT), Jiuzhen (JZ), Gangwei (GW), and Zhao’an (ZA) were in the range of 32−34 psu and 7.90−8.06, respectively, and they were not significant (p > 0.5). Received: Revised: Accepted: Published: 7050

January 12, 2014 June 20, 2014 July 6, 2014 July 7, 2014 dx.doi.org/10.1021/jf5001953 | J. Agric. Food Chem. 2014, 62, 7050−7056

Journal of Agricultural and Food Chemistry

Article

Table 1. Analytical Results for Metal in Oysters and Standard Reference Material (n = 3) standard oyster (NCSZC85007)

oyster

certified values (μg/g)

average results (μg/g)

RSD (%)

found (μg/g)

added (μg/g)

recovery (%)

370.9 139.7 6.67 4.56 0.84

360.2 ± 6.3 131.2 ± 1.3 6.1 ± 0.34 4.24 ± 0.20 0.78 ± 0.08

3.0 6.5 9.3 7.5 7.7

1310 ± 80 388.24 ± 2.1 17.48 ± 0.72 6.39 ± 0.32 2.46 ± 0.11

1300 388.00 17.00 6.00 2.50

105.2 106.1 101.2 99.3 99.8

Fe Cu As Cd Pb

Table 2. Total Phosphorus and Nitrate Nitrogen of Seawater in Gangwei, Zhao’an, Jiuzhen, and Fotan (mg/L, Mean ± SD; n = 3) total phosphorus nitrate nitrogen

GW

ZA

JZ

FT

0.015 ± 0.004 0.164 ± 0.032

0.035 ± 0.006 0.182 ± 0.040

0.034 ± 0.008 0.280 ± 0.042

0.043 ± 0.010 0.419 ± 0.046

Young small size oysters were transplanted to these four bays (FT, JZ, GW, and ZA) and a 4-month experiment was conducted from last December, 2012 to March, 2013. A batch of oysters (30 individuals) about 5 cm were collected and brought to the laboratory immediately and thoroughly cleaned again to eliminate organic materials and appendiculate sediments. The soft tissues were isolated from the shell, dried, and ground as a powder by an agate mortar. Preparation of Digestive Juices and Incubation of Gut Microbiota. The preparation of digestive juice and the incubation of gut microbiota were based on the reference.15 According to human physiology, the process and time of digestion were designed.16 The gastrointestinal inorganics, organics, bioenzyme, and gut microbiota were added to prepare the digestive juices. Oyster (1.0 g) powder was digested successively in the bionic mouth, stomach, and intestine at 37 °C on a gentle oscillation as follows. The bionic gastrointestinal digestion process was initiated with the addition of 5 mL of saliva and oscillated for 5 min to simulate chewing. Then, 30 mL of gastric juice was added to the above sample and incubated for 3 h to simulate bionic gastric digestion. After gastric digestion, the pH value of the chyme was adjusted to 7.8 ± 0.2 with 1 mol/L NaOH, and then the chyme was mixed with 30 mL of duodenal juice, 15 mL of bile, and 15 mL of gut microbiota, and incubated on a gently rocking shaker for 7 h to simulate for intestinal digestion. All chymes were filtered with a 0.45 μm membrane. Egg-derived (0.1 g) lecithin was dissolved in chloroform and then transferred into a rotatory evaporator to evaporate chloroform. Chyme (25 mL) was mixed with liposome to form a homogeneous liposome suspension, frozen at −71 °C in a super low freezer for 30 min, and then thawed at 37 °C. Such a freeze−thaw process was repeated 5 times to promote the metal speciation distribution in a liposome− water system. Affinity-liposome metals could be separated from watersoluble metals by 0.22 μm membrane. Determination of Metal Concentration in Seawater, Oysters, and Affinity-Liposome Metal in the Chyme. Oysters (0.1 g, powder) were added to concentrated HNO3 (4.0 mL) and Milli-Q water (4.0 mL), heated in a water bath at 80 °C until no smoke arose. Then, they were digested by concentrated HNO3 (2.0 mL) and H2O2 (1.0 mL, 30%) in closed Teflon tubes for 10 min, using a microwave technique. Seawater which has been filtered by a 0.22 μm membrane, all of the affinity-liposome metal, or water-soluble metal was directly decomposed by concentrated HNO3 (2.0 mL) and H2O2 (1.0 mL, 30%) in a microwave oven at the same conditions. After digestion, a dilution by water to 50 mL was carried out for metal determination by ICP-MS. Statistical Analysis. SPSS 19.0 was used for the statistical analysis. Possible relationships between trophic status (nitrate N or total P) and metal content (or metal BAF or metal OBA) were examined by partial correlation analysis and quantified by the coefficient of determination, r. A significance level of p < 0.05 was adopted for all comparisons. The regressions were quantified by the coefficient of determination, R2.

The plots and regression lines were drawn in SigmaPlot for Windows, version 10.0. Accuracy of the Method. The validity of the proposed method was checked by analyzing standard reference materials, and the results are shown in Table 1. The recoveries were reasonable for the analysis of Fe, Cu, As, Cd, and Pb in oysters, ranging from 99.3.−105.2%. Metal values were in good agreement with certified concentrations in both standard reference materials. The RSD was within 9.3%. Therefore, the described method can be applicable to the determination of low levels (mg/kg or mg/L) of metals (Fe, Cu, As, Cd, and Pb) in oysters, affinity-liposome metals, and those that are water-soluble in chyme.

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RESULT Trophic Status of Four Bays. Total phosphorus and nitrate nitrogen as trophic indicators of the bays in GW, ZA, JZ, and FT were determined and shown in Table 2. The bays of GW, ZA, JZ, and FT were semiclosed, the field experiment was done in winter (from December, 2012 to March, 2013), the seawater exchange rates were poor, and the concentration of N and P in the seawater was stable during our field experiment. These results were similar to those in the database from the Department of Ocean and Fisheries in Zhangzhou City, Fujian Province, China. Similar results were also reported for other semienclosed bays.17,18 Total phosphorus and nitrate nitrogen in these four bays were varied from 0.016 to 0.043 mg/L and from 0.164 to 0.419 mg/L, respectively. On the basis of the seawater quality standard of China, except for GW, the trophic status of the other three bays was eutrophication in some ways. Metal Bioaccumulation in Oysters and the Correlation of BAF and Trophic Status in Four Bays. Metal bioaccumulation in oysters under different trophic status is shown in Table 3. In seawater, the concentrations of these trace metals, except for Fe, were in the range of 0.11−6.53 μg/L; however, Fe content was from 0.26 to 2.11 mg/L. All metal contents in the seawater met the standard of clean bays. Fe contents in oysters ranged from 1.22 mg/g to 2.54 mg/g, and the other metals (Cu, As, Cd, and Pb) in oysters were enriched at the level of microgram per gram. Trace metals (Fe, Cu, As, Cd, and Pb) were largely bioaccumulated in oysters. BAF was used to evaluate metal bioaccumulation in oysters, which was significantly different (p < 0.001). Compared to the clean bay of GW, BAF in oysters was largely increased by 5.5 and 7.3 times for Fe in the trophic bays of JZ and FT, deceased by 0.5 times for Fe in trophic ZA, and 0.5−0.9 times for Cu in trophic ZA, JZ, and FT. However, the BAF of As was irregularly fluctuant, which did not relate to trophic status in seawater. The 7051

dx.doi.org/10.1021/jf5001953 | J. Agric. Food Chem. 2014, 62, 7050−7056

BAF of Pb did not vary significantly. Compared with the clean GW bay, the BAF of Cd in trophic bays (ZA, JZ, and FT) was decreased by 0.4−0.8 times. Furthermore, the BAF of Cd was increased as the trophic status, and the effect of trophic status on metal bioaccumulation could be discussed by partial correlation. Partial correlation between BAF of Cd and total P (or nitrate N) was highly significant (r = 0.999, p = 0.024 for total P; and r = 0.998, p = 0.035 for nitrate N). The BAFs of Cu and Pb in oysters were not significantly correlated (p > 0.05) with total P (r = −0.98, r = −0.93) or nitrate N (r = 0.96, r = 0.95). The BAF of Fe in oysters was not significantly correlated with nitrate N (r = 0.90, p > 0.05) and show no correlation with total P (r = −0.277). The bioaccumulation in oysters in four bays was significantly different (P < 0.01), but it was not correlated with total P or nitrate N. Relationship between Trophic Status of Seawater and Metal Oral Bioavailability. Only metal bioaccumulation in oysters could not fully reflect the potential toxicity or nutrition of metals in oysters. Therefore, metal oral bioavailability in oysters was studied by bionic digestion and liposome extraction. After bionic digestion, metal complexes in oysters could be released and entered into the gastrointestinal tract, transformed into their final coordinated complexes by the functions of bioemzymes and gut microbiota. The affinityliposome metals in the chyme were available for gastrointestinal absorption. Correlations of metal oral bioavailability in oysters and total P (or nitrate N) are shown in Figures 1 and 2, respectively. Oral bioavailability of trace metals (Fe, Cu, As, Cd, and Pb) in oysters was all below 24%, i.e., metal species distribution in the chyme of oysters was mainly water-soluble metals. Metal OBA in oysters was not beyond 3.9% for Cu, 8.0%−17.4% for Fe, and 7.7%−18.6% for Cd. Only a small fraction of Cu in oysters was absorbed by the bionic membrane. OBA of As in oysters under different trophic status ranged from 2.5% to 23.5%. OBA of Pb in oysters were ranged from 12.1% to 14.0%, which was not significant variation (two way analysis of variance, p = 0.15). With the aggravation of eutrophication, As OBA in oysters was largely increased. The OBA of As was significantly positively correlated to nitrate N (R2 = 0.973, P = 0.007) and total P (R2 = 0.904, P = 0.049). The OBA of Fe was negative correlated to nitrate N (R2 = 0.882, p = 0.061). However, the OBA of other metals did not show any correlation with total P or nitrate N (correlation significant at P > 0.05). Safety Assessment of Oysters for Consumption Based on Metal Oral Bioavailability. Deficiency of essential metals or metal overload is harmful for human health. Oysters are a kind of widespread seafood. Hence, safe dosage and maximum consumption of oysters are important for people. The impact of coastal trophic status on the metal safety of oysters should be assessed. Maximum consumption value for oysters was calculated by the ratio of tolerable upper intake levels (or maximum level of daily intake)19,20 to affinity-liposome metal content, and the results are shown in Table 4. The result demonstrated that the maximum level of daily intake of oysters was mainly controlled by affinity-metal content of As. The oyster’s maximum levels of daily intake ranged from 132.3 g/d to 197.4 g/d. As the N and P content increased, the maximum consumption of oysters was significantly decreased. Metal safety assessment of oysters demonstrated that an oyster’s quality was significantly influenced by coastal trophic status. Consequently, the contents of N, P, and metals in the coastal

Note: the density of seawater (ρw) was 1.025 g·cm−3. Metal bioaccumulation factor (BAF) was estimated by proportion of the oysters’ and water’s mass concentration. BAF = Conc.o × (Conc.w × ρw)−1; Conc.o and Conc.w stand for the concentrations of seawater and oyster, respectively.

BAF

Article

a

2.52 ± 0.13 155.81 ± 1.3 5.79 ± 0.28 3.00 ± 0.24 2.42 ± 0.10 0.06 0.22 0.33 0.03 0.20 ± ± ± ± ± 0.26 2.40 1.29 0.11 3.82 7299 40162 6291 24926 602 2.54 ± 0.11 109.24 ± 1.1 9.50 ± 0.35 3.39 ± 0.26 3.09 ± 0.16 0.08 0.21 0.45 0.03 0.30 ± ± ± ± ± 0.34 2.65 1.47 0.14 5.00 565 11305 3609 7996 352 1.22 ± 0.09 75.63 ± 0.8 16.71 ± 0.66 2.34 ± 0.21 2.21 ± 0.09 0.20 0.40 0.41 0.05 0.33 ± ± ± ± ± 2.11 6.53 4.52 0.28 6.13 1120 128556 4212 49535 596 1.31 ± 0.08 388.24 ± 2.1 17.48 ± 0.72 6.39 ± 0.32 2.46 ± 0.11 0.16 0.25 0.44 0.03 0.21 ± ± ± ± ± 1.14 2.95 4.05 0.13 4.03 Fe × 10−3 Cu As Cd Pb

conc. of oyster (μg/g) Cs (μg/L)

Co (μg/g)

BAF

Cs (μg/L)

conc. of oyster (μg/g)

BAF

conc. of seawater (μg/L)

conc. of oyster (μg/g)

BAF

conc. of seawater (μg/L)

FT JZ ZA GW

Table 3. Metal Concentration of Seawater in Oysters in JZ, FT, ZA, and GW and BAF (n = 3)a

9333 63337 4386 27778 617


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Figure 1. Relationship between the content of total phosphorus in seawater and metal oral bioavailability in oysters (two-tailed, partial correlation, n = 3).

and their debris) and dissolved metals in seawater.28,29 The increase of N and P concentration was associated with increasing algal abundance and debris. 27 Because the bioconcentration factors of metals by marine algae were different for different metal species and nutrient regimes,4 the influence of trophic status on metal BAF in oysters was also different with metal species. Increase of algal biomass or metal sedimentation in the debris in trophic bays may promote the ingestion of marine alga and debris. In our study, a significant positive effect of the trophic status of the seawater on the concentration of Cd in oysters (i.e., BAF) was observed. Consequently, the dominating assimilation pathway for Cd in oysters may be particulate ingestion. After gastrointestinal digestion and gut metabolism of oysters, the affinity-liposome metals in the chyme were bioaccessible to the gastrointestinal tract, so they could be

seawater should be monitored simultaneously to avoid metal toxicity in oysters for consumption.

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DISCUSSION In coastal ecosystems, eutrophication has become a serious environmental problem.21,22 The effect of trophic status on the metal bioaccumulation of an aquatic organism, such as crayfish23 and fish,24,25 has been reported. The input of macronutrients can not only change the concentration and ratio of marine nutrients but also affect algal structure (including species composition and abundance),26 growth, cell shape, surface basic function groups, and biochemical compositions.4 Coastal eutrophication also affected metal uptake and assimilation by marine algae and metal transfer in coastal food webs.3,27 Oysters, as suspension-feeding bivalves, could assimilate metals from two sources, food particulates (e.g., algae 7053



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Figure 2. Relationship between the content of nitrate nitrogen in seawater and metal oral bioavailability in oysters (two-tailed, partial correlation, n = 3).

Table 4. Maximum Level of Daily Intake for Oystersa

Furthermore, the interaction of nitrogen and the food web may influence the metal speciation in organisms. In natural waters, the biosynthesis of organoarsenicals was enhanced by eutrophication, and arsenic speciation would be influenced by the balance of biological processes.31 Metal ligands were closely related to metal oral bioavailability.32 As and Fe were mainly distributed in heat-stable protein and granules, respectively, in marine molluscs (including oysters).33 Subcellular distribution (including heat-stable protein and granules) of metal in marine oysters could be affected by the trophic status of seawater.34 In our experience, the OBA of As was positively related to the trophic status of seawater, i.e., the OBA of As in oyster was increased as the aggravation of eutrophication in seawater and the OBA of Fe in oyster was negatively correlated to nitrate N. Metal bioaccumulation and oral bioavailability in oysters were significantly different. Through the Pearson correlation analysis,

maximum consumption of oysters

Fe Cu As Cd Pb

Uls/ML value (mg/d)

GW (g/d)

ZA (g/d)

JZ (g/d)

FT (g/d)

45 10 0.18b 0.3 0.3

197.4 954.0 411.9 545.9 1007.9

256.1 3390.3 139.9 3561.3 969.6

221.5 7628.5 140.4 475.8 724.5

210.1 2917.3 132.3 1298.7 953.6

a

Note: Uls, tolerable upper intake levels; ML, maximum level of daily intake without detriment to health. bUIs of inorganic arsenic BMDL was computed to be 0.18 mg/d for 60 kg weight people (3.0 μg/kg body weight per day) by WHO.

refined as the metals which were orally bioavailable to humans. Metal oral bioavailability was controlled by organic ligands.30 7054



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only BAF of Fe was not significantly negative correlated to oral bioavailability (r = −0.992, P = 0.078). Consequently, this study suggested that As OBA in oysters could be used as a predictor of eutrophication in seawater and the potential toxicity of oysters for consumption. In previous studies, metal bioaccessibility was indicated as the metal fraction of seafood which was released from seafood into the digestive tracts. Only the fraction of bioaccessible metals which could be absorbed by the biomembrane of the gastrointestinal tract was oral bioavailable metals. The concentration of bioaccessible metal was more than that of oral bioavailable metal and metal exposure via the consumption of seafood could be overestimated by this difference.

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AUTHOR INFORMATION

Corresponding Author

*Tel: +86 596 2591395. Fax: +86 596 2591395. E-mail: [email protected]; [email protected]. Funding

This work is supported by the National Natural Science Foundation of China (41206096, 20775067, and 21175115), the Program for New Century Excellent Talents in University (NCET-110904), Outstanding Youth Science Foundation of Fujian Province, China (2010J06005), and the Science & Technology Committee of Fujian Province, China (2012Y0065). Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED BAF, bioaccumulation factor; OBA, oral bioavailability; FT, Fotan; JZ, Jiuzhen; GW, Gangwei; ZA, Zhao’an

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REFERENCES

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