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Comparison of bioavailability and biotransformation of inorganic and organic arsenic to two marine fish Wei Zhang, Wen-Xiong Wang, and Li Zhang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b06307 • Publication Date (Web): 02 Feb 2016 Downloaded from http://pubs.acs.org on February 2, 2016

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Environmental Science & Technology

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Comparison of bioavailability and biotransformation of inorganic and organic arsenic to two marine fish

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Wei Zhanga, Wen-Xiong Wangb, Li Zhanga*

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Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key

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Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese

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Academy of Sciences, Guangzhou 510301, China

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Division of Life Science, State Key Laboratory of Marine Pollution, Hong Kong University of Science and Technology (HKUST),Clearwater Bay, Kowloon, Hong Kong, China

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*Corresponding author

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Li Zhang, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou

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510301, P. R. China

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Tel: +86-20-89221322; Fax: +86-20-84452611

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E-mail address: [email protected]

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ACS Paragon Plus Environment


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ABSTRACT: Dietary uptake could be the primary route of arsenic (As) bioaccumulation in

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marine fish, but the bioavailability of inorganic and organic As remains elusive. In this study, we

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investigated the trophic transfer and bioavailability of As in herbivorous rabbitfish

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Siganus fuscescens and carnivorous seabass Lateolabrax japonicus. Rabbitfish were fed with one

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artificial diet or three macroalgae, whereas seabass were fed with one artificial diet, one

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polychaete, or two bivalves for 28 days. The six spiked fresh prey diets contained different

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proportions of inorganic As [As(III) and As(V)] and organic As compounds [methylarsenate

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(MMA), dimethylarsenate (DMA), and arsenobetaine (AsB)], and the spiked artificial diet

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mainly contained As(III) or As(V). We demonstrated that the trophic transfer factors (TTF) of As

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in both fish were negatively correlated with the concentrations of inorganic As in the diets, while

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there was no relationship between TTF and the AsB concentrations in the diets. Positive

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correlation was observed between the accumulated As concentrations and the AsB concentrations

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in both fish, suggesting that organic As compounds (AsB) were more trophically available than

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inorganic As. Furthermore, the biotransformation ability of seabass was higher than that in

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rabbitfish, which resulted in higher As accumulation in seabass than in rabbitfish. Our study

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demonstrated that different prey with different inorganic/organic As proportions resulted in

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diverse bioaccumulation of total As in different marine fish.

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Keywords: Arsenic; Trophic transfer; Bioavailability; Biotransformation; Marine fish

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INTRODUCTION Arsenic (As) is a pervasive environmental toxin with worldwide human health implications

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and its contamination in the environment has been widely reported. 1, 2 Arsenic is widely

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distributed in all organisms, 3 and total As concentrations in marine fish are higher (1–10 μg/g)

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than those in freshwater fish (90%), independent of the As speciation in the diet.

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Moreover, the AsB proportion of total As in diets and different tissues followed the order of

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diets< intestine ≤ liver < muscle (Supporting Information, Figure S1). In addition, in all exposed

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treatments of rabbitfish except As(V) exposed artificial diets treatments and artificial diets

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exposed treatments of seabass, the accumulated concentrations of AsB in the tissues followed the

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pattern of diets < intestine < liver < muscle (Table 1; Supporting Information, Table S2; Table

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S3). For instance, in the As(III) exposed G. lemaneiformis treatment for rabbitfish, through

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calculation, ingestion rate was maintained constant at about 3% of fish body weight. The total

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input of AsB through feed was 16.04 g (wet weight) ×3%×28 d×0.11 μg/g (AsB concentration in

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food) =1.48 μg. If we assumed that the assimilation efficiency was 100% at the end of 28 d

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exposure, the accumulated AsB concentration was 1.48 μg/17.9 g (wet weight by the end of 28

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d)=0.083 μg/g, but the detected AsB concentration in muscle of rabbitfish was 1.97 μg/g.

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Therefore, these results strongly suggested that biotransformation of As occurred in marine fish.

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For simplicity, we compared the ratio of organic As to inorganic As in different tissues to

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contrast the differences in biotransformation. Such ratios in different tissues of seabass were

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relatively higher than those in rabbitfish, suggesting that the conversion ability in seabass was

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higher than that in rabbitfish (Figure 1 C and D). For example, in the As(V) exposed artificial

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diet in which the predominant form of As was As(V), while the ratios of organic As to inorganic

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As were 0.72, 3.18, 8.84 in intestine, liver, and muscle tissues of rabbitfish, and those were 11.75,

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14.35, 14.75 in intestine, liver, and muscle tissues of seabass, respectively.

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DISCUSSION Bioavailability of Inorganic and Organic Arsenic in Fish. In our study, three tissues of

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rabbitfish and seabass displayed no significant correlation between inorganic As concentrations

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in fish and those in diets, except inorganic As in the intestine of rabbitfish. One possibility was

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that inorganic As was transformed to organic As in the fish. In contrast, AsB in carnivorous

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seabass was strongly correlated with those in diets (containing major AsB), indicating that AsB

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was more trophically available (bioavailable) than inorganic As. One likely explanation for such

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a correlation was that AsB was the final storage form of As in the fish tissues. Very few earlier

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studies have compared the bioavailability of inorganic vs. organic As. Kirby and Maher 33

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investigated the accumulation and distribution of As compound in marine fish species in relation

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to their trophic position. They speculated that As compounds present in fish tissues may be

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different depending on trophic position (diet) and/or their association with marine sediments.

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Pelagic carnivorous fish species exposed mainly to AsB through their diet accumulated this

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compound in their tissues.14, 34 However, the intestine of rabbitfish displayed significant

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correlation between inorganic As concentrations in fish and those in diets, mainly because

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intestine was the extrinsic digestive part, which was likely influenced by the surrounding

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environment (or biotransformation was low).

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We observed an inverse relationship between the TTF and inorganic As concentrations in diets.

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Inverse correlations between the TTF and metal (such as Cd, Pb and Zn) concentrations in prey

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were previously found in juvenile fish T. jarbua and rainbow trout Oncorhynchus mykiss35, 36, but

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such correlation had not been tested for inorganic As. The potential for metal trophic transfer can

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be described by the equation: TTF= (AE × IR)/ke, where AE represents the assimilation

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efficiency from ingested prey, IR is the ingestion rate of the predator, and ke is the efflux rate

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constant. This equation expressed theoretically the positive relationship between TTF and AE or

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IR but a negative relationship with ke. In this study, IR was maintained constant at about 3% of

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the body weight. Therefore, any change in TTF was likely due to changes of AE and ke. A lower

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TTF at a higher inorganic As burden suggested a somewhat less complete digestion and

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assimilation in the fish or more efficient elimination of As. One possible mechanism was that

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inorganic As was less efficiently assimilated by the limited number of transporters on the

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intestine epithelium. Alternatively, the biotransformation process may influence the assimilation

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of inorganic As. At high external inorganic As concentrations, biotransformation may be

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facilitated when inorganic As uptake became saturated. Whaley-Martin et al.37 found that high

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proportions of inorganic As might result from saturation of biochemical pathways responsible for

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the transformation of inorganic arsenicals (from food, water, and /or sediment) into AsB and

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other complex organoaresenicals. Earlier studies reported that once inorganic As was inside the

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cells, As(V) was removed by several reactions and transformations, including competition with

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phosphate, binding to polyphosphates (i.e., adenosine diphosphate, ADP), hydrolysis, and

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enzymatic reduction. 38, 39 Thus, reduction in TTF with increasing exposure concentration

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appeared to be driven mostly by changes in As AE or biotransformation instead of elimination.

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There was no relationship between TTF and AsB concentrations in diets, suggesting that TTF

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was not influenced by the AsB burden. Presumably, these compounds passed more easily

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through the apical membranes of the epithelial cells of the digestive organs than inorganic As. It

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is possible that AsB is taken up via the glycine betaine transport system of marine fish, and does

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not participate in metabolism processes. In other words, the marine fish receiving AsB in their

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diets accumulated As in this form without further metabolizing it. Thus, our present study

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demonstrated that As transfer along the food chain was influenced by prey types containing

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different As species, in which AsB was assimilated more easily than inorganic As along the food

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chain. Very few studies have quantified the bioavailability of inorganic As and organic As in

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marine fish. Earlier studies have simply reported the As bioaccumulation in organisms following

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dietborne As exposure. For instance, yelloweye mullet Aldrichetta forsteri fed upon a range of

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As compounds had low retention of As(V) in their muscle tissues, whereas fish that received

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either AsB or AsC had elevated levels of As in their muscles. 40

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In our study, As did not biomagnify in the marine fish, consistent with earlier studies in

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aquatic food chain. 14, 15, 18, 41, 42 Maher et al. 14 found no evidence of biomagnification of As in

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two Zostera capricorni seagrass ecosystems. Zhang et al.18 suggested that As did not biomagnify

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in a marine juvenile fish T. jarbua due to the very low AE and the relatively high ke. However,

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feeding on different diets might affect As biomagnification potential in marine fish.

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Biomagnification can occur in some ecosystems as evidenced by gastropods in rocky intertidal

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systems. 43

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After dietary exposure, the bioavailability of AsB was higher than inorganic As, and AsB

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contributed to the accumulation of total As in marine fish. Hong et al. 44 investigated the in situ

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bioaccumulation of As in various aquatic organisms in a highly industrialized area of Pohang

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City, Korea. AsB was the most dominant form of As in fish, bivalves, crabs, and shrimps, and

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was directly proportional to the total concentration of As in their tissues. In our study, positive

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correlation was observed between the newly accumulated As concentration and the ratio of

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organic As (subtracting the background concentrations)/inorganic As in seabass (Supporting

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Information, Figure S2). Thus, following the absorption in the intestine, the bioaccumulation of

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As compounds may be altered by biotransformation, leading to dramatic changes in the

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bioaccumulation. Therefore, As biotransformation could influence the bioaccumulation of As in

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marine fish.

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Arsenic Bioaccumulation and Biotransformation in Fish. Our study demonstrated that the

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potential of As bioaccumulation in seabass was higher than that in rabbitfish. Such high

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bioaccumulation in carnivorous seabass may be attributed to its prey types. Different prey

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contained different proportions of inorganic As and organic As compounds, and the diets of

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seabass contained more AsB than rabbitfish. AsB could be more efficiently transmitted than

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inorganic As along the food chain. Therefore, our findings again confirmed the relative

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significance of prey type in regard to As bioaccumulation in marine fish. The observed

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interspecific differences in wild-caught fish found in previous studies may be explained by

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differences in diet among species. 45 The herbivorous cyprinids and carnivore fish species

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exhibited significantly different abilities to accumulate As in their body organs, with the

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maximum As concentration of 4.01 µg/g recorded in a carnivorous fish Wallago attu, and the

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minimum one (2.12 µg/g) in a herbivorous fish Catla catla. 46 Therefore, variation of As

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concentration among fish species could be attributed to prey type including different As species.

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On the other hand, such high bioaccumulation may be explained by the higher

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biotransformation ability in seabass than that in rabbitfish. When both fish feeding on artificial

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diets containing mainly As(V), for example, more As(V) was biotransformed into organic As by

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seabass, leading to more As accumulated in seabass compared with rabbitfish. The fish may

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adapt and regulate when different As species pass through the body. One possibility is that they

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biotransform As to less toxic forms or reduce the toxic As accumulation, which may be

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responsible for the higher bioaccumulation in seabass than that in rabbitfish. Cockell 47 reported

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that with continued exposure to dietborne As, epithelial cells in the hepatobiliary system must

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undergo an adaptation in order to allow them to regenerate. Such adaptation may occur by the

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increase of metabolic transformation of As to a less toxic form, or the reduction of net

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accumulation by decreasing uptake or increasing excretion of As. Until now, limited data have

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been available for the comparison of bioaccumulation with some information of

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biotransformation. Therefore, it would be interesting to use radiotracer studies to quantify the

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relationship between As bioaccumulation and As speciation in a future study.

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This study examined the trophic transfer and bioavailability of As in two typical marine fish,

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herbivorous rabbitfish and carnivorous seabass feeding on different prey types with different

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proportions of inorganic As and organic As compounds. We demonstrated that different diets had

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significant effects on As bioavailability and bioaccumulation in marine fish. The bioavailability

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of AsB was higher than that of inorganic As. Inorganic As in both fish was difficult to be

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transmitted along the food chain, due to their biotransformation in the fish tissue rather than

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direct accumulation. While AsB was more assimilated than inorganic As, possibly because AsB

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passed more easily through the apical membranes of the cells of the digestive organs, and was

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the final storage form of As in the fish tissues. Therefore, differential bioavailability of inorganic

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and organic As contributed to their different bioaccumulation in marine fish.

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Supporting Information

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The AsB distribution (%) in exposed diets and different tissues of rabbitfish and seabass after

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different exposed treatments for 28 d, the correlation between newly accumulated As

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concentrations and the ratio of organic As/inorganic As in seabass, total As, As species

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concentrations and distribution (%) in unspiked food, As species concentrations in intestine, liver,

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and muscle tissues of marine rabbitfish and seabass. This information is available free of charge

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via the Internet at http://pubs.acs.org.

ASSOCIATED CONTENT

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Corresponding Author

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*

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Notes

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The authors declare no competing financial interest.

AUTHOR INFORMATION

Phone: 86-020-89221322. E-mail: [email protected]

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This work was supported by National Natural Science Foundation of China (21407156,

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41376161), The State Key Development Program for Basic Research of China (2015CB452904),

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the 100 Talents Project of Chinese Academy of Sciences, Science and Technology Planning

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Project of Guangdong Province, China (2014B030301064).

ACKNOWLEDGMENTS

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Figure legends

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Figure 1. Comparison of the As concentrations (μg/g) in rabbitfish (A) and seabass (B) after

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As(V) exposed artificial diet exposure. Data are means±SD (n=18–20). The ratio of organic As

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and inorganic As in intestine, liver, and muscle tissues of rabbitfish (C) and seabass (D) after

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different dietborne exposure for 28 d. The foods contain artificial diets, red algae G.

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lemaneiformis, G.gigas, green algae U. lactuca, polychaete N. succinea, oyster S. cucullata, and

507

clam A. violascens. Data are means±SD (n=3). *represent significant differences between control

508

and treatment (p

Comparison of Bioavailability and ... - ACS Publications

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