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Quantifying Bioavailability of Pyrene Associated with Dissolved Organic Matter of Various Molecular Weights to Daphnia magna Hui Lin, Xinghui Xia, Siqi Bi, Xiaoman Jiang, Haotian Wang, Yawei Zhai, and Wu Wen Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b05520 • Publication Date (Web): 14 Dec 2017 Downloaded from http://pubs.acs.org on December 15, 2017
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Quantifying Bioavailability of Pyrene Associated with Dissolved Organic
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Matter of Various Molecular Weights to Daphnia magna
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Hui Lin, Xinghui Xia*, Siqi Bi, Xiaoman Jiang, Haotian Wang, Yawei Zhai, Wu Wen
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School of Environment, Beijing Normal University, State Key Laboratory of Water Environment Simulation,
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Beijing 100875, China
6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 *
Corresponding author. Tel./fax: +86 10 58805314.
E-mail address:
[email protected] (X. Xia) 1
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ABSTRACT
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Dissolved organic matter (DOM) is a key environmental factor for the bioavailability of
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hydrophobic organic compounds (HOCs) in natural waters. However, the bioavailability of
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DOM-associated HOCs is not clear. In this research, pyrene was selected as a model HOC and its
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freely dissolved concentration (Cfree) was maintained by passive dosing systems. The
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immobilization and pyrene content in the tissues excluding gut of Daphnia magna were examined
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to quantify the bioavailability of DOM-associated pyrene. The results indicated that DOM
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promoted the bioavailability of pyrene when the Cfree of pyrene was kept constant, and the
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bioavailability of pyrene associated with DOM of various molecular weights was ordered as
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middle molecular weight (5-10K Da) DOM > lower molecular weight ( higher molecular weight (>10K Da) DOM. The influencing mechanisms of
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DOM molecular weight were related with the partition of pyrene between DOM and water, the
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uptake routes of DOM by Daphnia magna, and the desorption or release of pyrene from DOM in
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the gut of Daphnia magna. The findings obtained in this research suggest that the bioavailability
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of DOM-associated HOCs should be taken into account for the eco-environmental risk
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assessment of HOCs in water systems.
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Key words: Bioavailability; Dissolved organic matter (DOM); Molecular weight; Passive dosing
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systems; Immobilization; Freely dissolved concentration
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1. INTRODUCTION
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Hydrophobic organic compounds (HOCs) and their risks to the environment, organisms, and
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human health have aroused wide public concern for a long time. In natural waters, HOCs can be
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easily associated with dissolved organic matter (DOM) by various forms of binding and
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adsorption,1,2 such as hydrogen bonding, covalent bonds, hydrophobic interactions, and
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partitioning.3-8 The ubiquity of DOM in environments and its ability to sorb HOCs exert
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significant influence on the distribution, fate, and bioavailability of HOCs.9-12 For example, the
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distribution, fate, and bioavailability of polycyclic aromatic hydrocarbons (PAHs) are greatly
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influenced by DOM in natural waters.13,14
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Most of previous studies suggested the presence of DOM could decrease the freely dissolved
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HOC concentrations when the total dissolved concentrations of HOCs remain unchanged in water
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due to the binding of HOCs with DOM,15,16 and hence reduce HOC bioavailability and
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toxicity.17-19 For example, Perminova et al.20 found the toxicity of PAHs to Daphnia magna was
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alleviated by humic acids (HA) and fulvic acids (FA), and Yang et al.21 reported DOM at low
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levels (3-20 mg-C L-1) reduced the uptake of cyfluthrin by Daphnia magna. On the contrary, the
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enhancement of PFAS bioaccumulation by Daphnia magna after addition of DOM at a low level
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was found by Xia et al. because the uptake and elimination rates of PFAS in Daphnia magna were
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influenced by DOM.22 In addition, it has been reported that DOM can enhance the diffusive mass
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transfer of PAHs in the unstirred boundary layer, which is often seen as the rate limiting process
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for the PAH uptake in aquatic organisms.23,24 According to Ter Laak et al.,25 when
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benzo[b]fluoranthene was controlled at a low level, its accumulation by Lumbriculus variegatus
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increased after adding 55 mg-C L-1 HA resulting from the DOM-promoted transport of
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benzo[b]fluoranthene to organisms. There is also evidence that phenanthrene biodegradation rates
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were enhanced by adding HA in a saline mineral medium resulting from the HA-mediated
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transport of phenanthrene to the cells.26 Furthermore, previous research revealed microbes could 4
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degrade the DOM-associated HOCs directly.27 Divergent findings above indicate that the
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influence of DOM on the bioavailability of HOCs is not well understood, and the main reason for
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this is that the bioavailability of DOM-associated HOCs is not well studied and quantified.
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Dissolved organic matter is a complex and heterogeneous mixture, and its structural
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components are still elusive due in part to molecular complexity of DOM.28 Because the
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molecular weight of DOM is closely related to its functionality and source, the molecular weight
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distribution of DOM has been extensively investigated in natural waters including streams, lakes,
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rivers, and sea.29-32 Many studies suggest the sorption on and desorption of HOCs from DOM are
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related to DOM molecular weight.33,34 The larger molecular weight of DOM is, the bigger
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organic carbon normalized partition coefficient (Kdoc) of pyrene is.35,36 Furthermore, Xia et al.37
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reported the bioaccumulation of perfluorooctanoic acid by Daphnia magna was enhanced by 1
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mg-C L-1 HA or FA, and the increases of bioaccumulation factors resulted from HA and FA were
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66% and 24% respectively, which indicated the high molecular weight DOM (HA) exert stronger
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influence on the bioaccumulation of perfluorooctanoic acid than the low molecular weight DOM
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(FA). In addition, the lower molecular weight DOM could pass through the biomembrane of
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organisms more easily compared to the higher molecular weight DOM,38 and thus the HOCs
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associated with lower molecular weight DOM might be taken up by organisms directly.
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Accordingly, it is very reasonable to hypothesize that the bioavailability of DOM-associated
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HOCs will vary with DOM molecular weight.
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Therefore, the aim of this research was to quantify the bioavailability of HOCs associated
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with DOM of various molecular weights. Pyrene and Daphnia magna were chosen as model HOC
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and organism respectively in this work. The improved passive dosing devices39,40 were made to
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maintain the freely dissolved pyrene concentration (Cfree) stable in the systems containing DOM
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with various molecular weights including >10K Da, 5-10K Da, 3-5K Da, 1-3K Da, and 10K Da), F2
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(5-10K Da), F3 (3-5K Da), F4 (1-3K Da), and F5 (10K Da) solutions after exposure for 144 h which was only 36 h later compared to that in
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AFW. However, after exposure for 144 h, the immobilization of Daphnia magna was only 30%
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and 0-40% in 10 mg-C L-1 middle molecular weight DOM (MMW DOM, 5-10K Da) and lower
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molecular weight DOM (LMW DOM, HMW, with
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the bioavailable fractions being 41.8%, 27.7%-32.5%, and 16.1%, respectively after exposure for
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48 h when the DOM concentration was 30 mg-C L-1.
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In addition, based on the relationship between the immobilization of Daphnia magna and the 15
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freely dissolved pyrene concentration (Cfree, µg L−1) in the absence of DOM (Figure S9), we
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could deduce the effective concentration of pyrene (Ceffective(2), µg L−1)40 causing the observed
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immobilization of Daphnia magna in systems containing DOM. As mentioned above, the food
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effect of 10 mg-C L-1 DOM was the same as 30 mg-C L-1 DOM. Therefore, the higher
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immobilization of Daphnia magna in the systems containing 30 mg-C L-1 DOM was caused by
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the difference between the pyrene associated with 30 mg-C L-1 DOM and 10 mg-C L-1 DOM.
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Consequently, the bioavailable fraction of DOM-associated pyrene (FDOM(2), %) based on the
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immobilization of Daphnia magna could be quantified with the following equation:
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ܨୈ(ଶ) =
ౙ౪౬యబ(మ) ିౙ౪౬భబ(మ) [ୈ]యబ ×ీోయబ ି[ୈ]భబ ×ీోభబ
× 100%
(2)
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where Ceffective30(2) and Ceffective10(2) (µg L-1) were the effective concentrations of pyrene based on
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the immobilization of Daphnia magna in the systems containing 30 mg-C L-1 and 10 mg-C L-1
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DOM, respectively; [DOM]30 and [DOM]10 were 30 mg-C L-1 and 10 mg-C L-1 DOM in the
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systems, respectively; CDOM30 and CDOM10 (µg mg-1) were the concentrations of pyrene associated
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with DOM in the systems of 30 mg-C L-1 and 10 mg-C L-1 DOM, respectively. The obtained
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results are summarized in Table 1; the order of the bioavailable fraction of pyrene associated with
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DOM of various molecular weights was MMW > LMW > HMW. The bioavailable fractions of
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pyrene associated with MMW, LMW, and HMW DOM were 60.6%, 40.7%-48.9%, and 25.2%,
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respectively after exposure for 48 h when the DOM concentration was 30 mg-C L-1. They were
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higher than the results based on the pyrene content in tissues of Daphnia magna, and this
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suggested that DOM-mediated diffusive mass transfer effect and the indirect uptake of
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DOM-associated pyrene have promoted the accessibility of pyrene to Daphnia magna, enhancing
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the immobilization of Daphnia magna.
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3.5. Influencing Mechanisms of DOM Molecular Weight on the Bioavailability of
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DOM-Associated Pyrene to Daphnia magna
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3.5.1. Partition of Pyrene between DOM and Water 16
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The concentration of DOM-associated pyrene was highest in the HMW DOM solution,
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followed by MMW and LMW DOM solutions when the DOM concentration was identical in the
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systems; correspondingly, the Kdoc of pyrene between DOM and water was ordered as HMW >
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MMW > LMW (Table S5). For example, when the freely dissolved pyrene and DOM
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concentrations were 60 µg L-1 and 10 mg-C L-1 respectively, the LMW DOM-associated pyrene
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concentration was 3.04 × 106 - 3.57 × 106 µg kg-1, and the MMW and HMW DOM-associated
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pyrene concentrations were 5.90 × 106 and 1.10 × 107 µg kg-1 respectively; the Kdoc of pyrene in
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the systems with LMW DOM were 5.06 × 104 - 5.94 × 104 L kg-1, and that with MMW and HMW
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DOM were 9.84 × 104 and 1.84 × 105 L kg-1 respectively. In this research, the lg Kdoc of pyrene
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between DOM of various molecular weights and water ranged from 4.69 to 5.28, which were in
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the range (3.24-5.69) of the lg Kdoc values of pyrene between DOC of various types and water
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reported by Li et al.51
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3.5.2. Routes of DOM-Associated Pyrene Taken up by Daphnia magna
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The pollutants associated with DOM might be taken up by organisms through three routes:
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(1) transmembrane transport occurring on skin and gut wall; (2) endocytosis occurring on skin
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and gut wall; (3) desorbing from DOM or releasing from DOM degraded by digestive enzymes in
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the gut and taken up by organisms.52-54 Only pollutants associated with DOM of low molecular
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weight could be directly taken up by organisms through route (1). It is reported that LMW, however, the
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bioavailable fraction of pyrene associated with DOM was ordered as MMW > LMW > HMW.
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Since the bioavailable amount of pyrene was equal to the total amount of DOM-associated pyrene
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in the exposure solutions multiplied by the bioavailable fraction of pyrene associated with DOM,
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the net effect of Kdoc and bioavailable fraction led to that the pyrene content in the tissues of
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Daphnia magna excluding gut was the highest in the system of MMW DOM, followed by LMW
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DOM and HMW DOM when the freely dissolved concentration was identical as mentioned in
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section 3.3. It also resulted in that the additional immobilization caused by MMW DOM was
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higher than HMW DOM compared to the control group with only freely dissolved pyrene.
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3.6. Environmental Implications
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Many researchers suggest that the freely dissolved HOCs concentration is an indicator of
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bioavailability of HOCs. However, this study suggests that the DOM-associated pyrene was
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partly bioavailable to waterflea Daphnia magna, and the bioavailability of DOM-associated 19
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pyrene was influenced by the molecular weight of DOM. When freely dissolved pyrene
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concentration was 60 µg L-1, the pyrene content in the tissues of Daphnia magna in the systems
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containing 30 mg-C L-1 DOM with various molecular weights increased 42.1-92.2% compared to
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that in the control group without DOM. The results indicated that DOM-associated pyrene played
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an important role in the toxicity of pyrene in the exposure systems. Since DOM is ubiquitous in
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natural waters, it may not be suitable to consider the freely dissolved HOCs as the only
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bioavailable form; the bioavailability of DOM-associated HOCs should be taken into
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consideration in aquatic environments. Furthermore, the DOM concentration and structure will
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vary among the natural waters,56,57 and other water conditions including cations and pH values
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could influence the binding of HOCs to DOM.58,59 In addition, DOM effect on the bioavailability
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of HOCs also depends on the exposure regime.60 Consequently, the concentration, molecular
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weight, composition, and structure of DOM as well as other water conditions and the exposure
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regime should be considered when studying the bioavailability of HOCs in aquatic environments.
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The aquatic organisms are usually used to assess the bioavailability and toxic risks of HOCs
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in water systems. The utilization of DOM by organisms will depend on organism species with
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specific body length, body structures, and dietary habits, which will further influence the entry
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routes
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DOM-associated HOCs. Consequently, the organism species should be considered for the risk
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and bioavailability assessment of HOCs in water systems besides the DOM properties and water
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conditions, and more research should be conducted in this regard in the future. Especially, the
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direct uptake of DOM-associated HOCs by aquatic organisms needs further study.
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Supporting Information
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The Supporting Information is available free of charge on the ACS Publications website at DOI:
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of
DOM-associated
HOCs into organisms, thus affecting bioavailability of
Tables S1-S5 and Figures S1-S11 20
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Acknowledgements
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This work was supported by the National Key R&D program of China (2017YFA0605001),
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the National Natural Science Foundation of China (91547207), the National Science Foundation
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for Distinguished Young Scholars (51325902), and the National Natural Science Foundation for
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Innovative Research Group (51421065).
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658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 28
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Table 1. Bioavailable fraction of DOM-associated pyrene to Daphnia magna
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(Average of three replicates, RSD < 10%) Based on the pyrene content in the tissues of Daphnia magna
DOM molecular weight and concentration
Cfree of pyrene (µg L-1)
Bioavailable fraction of DOM-associated pyrene (%) 48 h
Based on the immobilization of Daphnia magna Cfree of pyrene (µg L-1)
Bioavailable fraction of DOM-associated pyrene (%) 36 h
48 h
10 K Da (30 mg-C L-1)
60.0
16.1
20.0
25.7
25.2
681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 29
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Immobilization (%)
100
20 µg L-1 pyrene Control 10K Da
80 60 40 20 0 0
Immobilization (%)
100
12
24
36
48
24
36
48
24
36
48
40 µg L-1 pyrene Control 10K Da
80 60 40 20 0 0
Immobilization (%)
100
12 60 µg L-1 pyrene Control 10K Da
80 60 40 20 0 0
707
12
Time (h)
708
Figure 1. Effects of DOM (10 mg-C L-1) with different molecular weights on the immobilization
709
of Daphnia magna at different freely dissolved pyrene levels during a 48-h exposure (mean ±
710
standard deviation, n = 3). Control means without DOM, and the immobilization of Daphnia
711
magna was zero in the solutions of DOM without pyrene during a 48-h exposure.
712
713
714
715
716 30
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100
-1
Immobilization (%)
20 µg L pyrene Control
80
-1
10 mg-C L DOM (5-10K Da) -1
30 mg-C L DOM (5-10K Da)
60 40 20 0 0 100
12
24
36
48
-1
Immobilization (%)
20 µg L pyrene Control
80
-1
10 mg-C L DOM (>10K Da) -1
30 mg-C L DOM (>10K Da)
60 40 20 0 0
12
24
36
48
Time (h)
717 718
Figure 2. Effects of MMW and HMW DOM concentrations on the immobilization of Daphnia
719
magna during a 48-h exposure. (mean ± standard deviation, n = 3). Control means without DOM,
720
and the immobilization of Daphnia magna was zero in the solutions of DOM without pyrene
721
during a 48-h exposure.
722
31
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100
-1
Immobilization (%)
60 µg L pyrene