Comparison of Bioavailability and Biotransformation of Inorganic and

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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

505

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

506

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 Biotransformation of Inorganic and

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