Dissolution of Sedimentary Polycyclic Aromatic Hydrocarbons into the

Environ. Sci. Technol. 2000, 34, 1221-1228

Dissolution of Sedimentary Polycyclic Aromatic Hydrocarbons into the Lugworm’s (Arenicola marina) Digestive Fluids IAN M. VOPARIL* AND LAWRENCE M. MAYER Darling Marine Center, University of Maine, Walpole, Maine 04573

We studied the mechanism(s) by which a deposit feeder can solubilize PAH from contaminated sediments as well as the implications of these mechanisms for factors controlling PAH bioavailability. Arenicola marina digestive fluids solubilize 4.6 µg mL-1 phenanthrene and 2.0 µg mL-1 benzo[a]pyrenesconcentrations greater than the PAH’s seawater solubilitiesswhen incubated with pure PAH solids. This enhanced solubilization is largely due to surfactant micelles in the digestive fluid. In experiments with contaminated sediments that repeat the incubation or vary the solid-fluid ratio, these and other PAHs saturate at much lower concentrations (often between 0.01 and 0.1 µg mL-1). Less solubilization is likely due to sorption of digestive surfactants by sedimentary organic matter and competition from other sedimentary hydrophobic solutes, such as aliphatic hydrocarbons, for remaining micellar space. Nevertheless, gut fluid concentrations of high molecular weight PAHs are greater than those predicted from equilibrium partitioning theory, indicating the importance of the digestive pathway for hydrophobic organic contaminant exposure and bioaccumulation.

Introduction Deposit feeders ingest great quantities of sediment that may increase exposure to and bioaccumulation of associated contaminants (1-3). Ingestion may be the principal pathway for the accumulation of polycyclic aromatic hydrocarbons (PAHs) with especially low aqueous solubilities, such as benzo[a]pyrene (4, 5). To better understand digestive solubilization of PAHs, in vitro incubations of contaminated sediment with digestive fluids extracted from various organisms have been performed (6-8). Gut fluids have been shown to release greater concentrations of sedimentary PAHs than seawater, presumably to a form more available for gut absorption; almost 100% of a radiolabeled PAH solubilized by Abarenicola pacifica gut fluid was also assimilated by the animal (7). A hydrophobic contaminant’s ability to cross a biological membrane depends in large part on the type of organic material with which the contaminant is associated. Freely dissolved contaminants are completely bioavailable (9), while those associated with dissolved organic matter (DOM) show reduced bioavailability (9-11). However, DOM is an assemblage of many different organic compounds that may * Corresponding author phone: (207)563-3146, ext.227; fax: (207)563-3119; e-mail: [email protected]. 10.1021/es990885i CCC: $19.00 Published on Web 02/25/2000

 2000 American Chemical Society

each have different effects on contaminant bioavailability. For example, DOM in sediment interstitial water is composed of humic substances and other geomacromolecular materials that are refractory and tend to complex organic contaminants in an unavailable form (10). The DOM in an invertebrate’s gut consists of different compounds; gut fluids have high levels of food hydrolysates, digestive enzymes, and surfactants (12). Presumably, digestion functions to render these compounds available for absorption; thus, it is premature to suggest that contaminants bound by digestive DOM are sequestered unavailable in the same way as contaminants associated with sedimentary DOM. Therefore, it is important to determine the type of digestive DOM responsible for the solubilization of contaminants. It was hypothesized that surfactants were responsible for enhanced digestive fluid PAH solubilization relative to seawater (6, 7) just as commercial surfactants enhance the solubility of hydrophobic organic compounds (13-15). In aqueous systems, surfactants at concentrations above the critical micelle concentration (cmc) aggregate to form micelles, nonpolar pseudophases that can absorb hydrophobic compounds. One way to test for micellar solubilization of PAHs is by measuring PAH solubilization by solutions with concentrations of surfactants both above and below the cmc; much greater concentrations of PAHs can be dissolved above the cmc (15). Gut fluid micellar solubilization of PAH does not necessarily result in bioavailable PAHs; e.g., humic-type compounds can form micelles that solubilize hydrocarbons (16) but are not bioavailable. The surfactants in marine invertebrate guts however are structurally very different from humic materials (ref 17 and R. Findlay, personal communication). During vertebrate mammalian digestion, which has been well-studied but may not be directly analogous to deposit feeder digestion, bile salt micelles shuttle lipids through the bulk aqueous solution to the digestive epithelium. Not only are lipids in bile salt micelles bioavailable but solubilization into micelles is required for efficient digestive assimilation (for review, see ref 18). In vivo, a deposit feeder’s digestive environment is pliant. Different sections of the digestive tract vary greatly in their surfactant, enzyme, and DOM concentrations (12) as well as in solid-fluid ratio (19). Digestive secretions may change with the age of the individual (12) and in response to the composition of the diet (20). This variability in the digestive environment will likely influence contaminant solubilization and bioavailability. There are three objectives of this study: (i) to determine if surfactant micelles in a deposit feeder’s gut fluids (A. marina) are responsible for solubilizing PAHs; (ii) to test for variability in PAH digestive availability in response to change in duration, solid-fluid ratio, and sequence of in vitro incubations; (iii) to compare gut fluid PAH exposure to another commonly used measure of bioavailabilitysequilibrium partitioning theory (9). In this paper, we will consider only the solubilization step and not the uptake of gut fluid contaminants across the digestive tract or metabolic transformations once inside the organism.

Materials and Methods Collection of Arenicola marina Gut Fluids. Arenicola marina (Linnaeus, 1758) (lugworm) individuals were collected from sandflats near Lubec, ME. Animals were stored in flowing seawater and sediment awaiting extraction of gut fluid for up to 3 days. Gut fluids were removed by carefully cutting open the body wall and inserting a pipet tip directly into the stomach. Gut section nomenclature of ref 19 is used in this VOL. 34, NO. 7, 2000 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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paper. Fluids from the stomach have maximal enzyme activity and surfactant concentration (12). Individuals’ fluids were pooled, centrifuged (1200g for 12 min) to remove mineral particles, decanted into plastic containers, and stored at -80 °C until use. Sediments. Sediments from three contaminated sites were used in this study: Little Mystic Channel, Charlestown, MA; Ft. Independence, South Boston, MA; and Pier 8, San Diego, CA. The first two sediments were collected by hand from intertidal regions at low tide, while Pier 8 sediment was collected at a subtidal station from a ship using a benthic grab. Within 1 day of collection, sediments were washed with 5% artificial seawater/DI water (by volume) followed by centrifugation at 8000g twice (to remove salt), freeze-dried, and stored in the dark at 5 °C. Sediment samples were analyzed for total organic carbon (TOC), after vapor-phase acidification to remove carbonates, by a Perkin-Elmer 2400-II CHN analyzer. Specific surface areas (SFA) of the mineral fraction were determined by singlepoint BET analysis using a Quantachrome Monosorb (21). The Massachusetts sediments were oxidized by 350 °C muffling and Pier 8 sediment underwent hydrogen peroxide oxidation to remove organic material prior to surface area measurement. Gut Fluid Incubations. Four types of incubation experiments were used to investigate PAH release to gut fluid: kinetics, gut fluid dilution to study PAH solubilization above and below the cmc, solid-fluid ratio, and repeat incubations of a single sediment sample with fresh aliquots of gut fluid. During experiments, gut fluids and sediment were incubated on a rotary shaker (120 rpm) in the dark because PAHs are photosensitive (22). All incubations were done in duplicate with each duplicate split into analytical duplicates, each undergoing cleanup separately, resulting in four data points for each sample. All incubations were for 4 h except for the kinetics experiment. Solid-fluid ratios reported throughout this paper are in g dry weight of sediment (mL of gut fluid)-1. Kinetics. Individual aliquots of a mixture of Little Mystic Channel sediment and gut fluid, at a solid-fluid ratio of 0.3 g mL-1 (typical of stomach), were incubated for 0.25, 0.5, 1, 2, 4, 8, 16, and 32 h. Dilution. Initial dilution experiments were performed with pure PAHs to assay gut fluid’s potential solubilizing capability. Then, dilutions of gut fluids were incubated with contaminated sediments to approximate more realistic substrates. Pure PAHs were incubated with three types of solutionssA. marina gut fluids, sodium dodecyl sulfate (SDS) solutions, and bovine serum albumin (BSA) solutions. Each was diluted with artificial seawater (without calcium for SDS). Dilutions of SDS (initial concentration of 2.0 mM) and BSA (initial concentration of 250 mM amino acids) served as models of surfactants and proteins at concentrations of each found in A. marina guts (12). Proteins make up the bulk of gut fluid DOM (unpublished data) and can absorb PAHs (23). Pure, solid PAH (0.4 g of benzo[a]pyrene or 0.2 g of phenanthrene) was incubated with 0.5 mL of dilutions of each type of solution. After incubation, solutions were clarified by centrifugation (1200g for 12 min) and filtration (0.45 µm filter). PAHs were extracted from the solution phase by chloroform overnight at 1 °C. PAH concentration in the chloroform was measured fluorimetrically using a Hitachi F-4500 fluorescence spectrophotometer at excitation/emission wavelengths of 280/ 360 nm for phenanthrene and of 370/430 nm for benzo[a]pyrene. To determine the importance of surfactant micellization for PAH solubility, we determined the critical micelle dilution (cmd), the dilution at which the critical micelle concentration is reached, using contact angle measurements of the various dilutions of gut fluid on Parafilm (12). The cmd was identified, 1222

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on plots of contact angle vs dilution, as a breakpoint between two linear segments of different slope after log-transformation of the dilution axis (24). Dilution experiments were also performed using gut fluids with each sediment at a solid-fluid ratio of 0.3 g mL-1. These gut fluids were purified, and PAHs were quantified as described below. Solid-Fluid Ratio. The effect of solid-fluid ratio was assessed by making slurries consisting of a fixed volume of gut fluid (1 mL) and a series of increasing amounts of sediment, from 0.015 to 1 g dry weight of sediment. Above a ratio of 1 g mL-1, it was prohibitively difficult to separate enough gut fluid from sediment for analysis. After incubation with various amounts of sediment, one subsample was subjected to PAH analysis. On another subsample, contact angles were again measured on gut fluids titrated with artificial seawater to determine changes in the fluid’s cmd. Repeat Incubation. All sediments were subjected to repeated incubations with fresh gut fluids to confirm PAH saturation behavior found in solid-fluid experiments as well as to examine the implications for multiple feeding events. After a first incubation (4 h), the mixture was centrifuged (1200g for 12 min), and 1 mL of gut fluid was removed for PAH measurement. One milliliter of fresh gut fluid was added to the sediment slurry, and the process was repeated for a total of five incubations. Pier 8 sediments were incubated at a solid-fluid ratio of 1.0 g mL-1 while Little Mystic Channel and Ft. Independence incubations, performed after the Pier 8 experiments, were done at a ratio of approximately 0.2 g mL-1. This change was made after solid-fluid ratio experiments indicated that PAH release leveled off at ratios above 0.2 g mL-1. We used a smaller amount of sediment in an attempt to quantify a “total” bioavailable fraction, i.e., to deplete the sedimentary PAH released to gut fluids after the first few incubations. PAH Analysis. Total Sedimentary PAH Extraction. To measure total sedimentary PAH, freeze-dried sediments were extracted with acetone:hexane (1:1 by volume) for 20 min at 115 °C in a microwave (CEM MSP 1000). Deuterated internal standards (phenanthrene-d10, benzo[a]anthracene-d12, and benzo[a]pyrene-d12) were added, and final PAH concentrations were adjusted for their recovery efficiency, which ranged from 88 to 117%. Extracts were stored overnight with reduced copper filings to remove sulfur compounds and purified and quantified as described below. Extraction of PAH from Digestive Fluid. Following incubation, the sediment-gut fluid slurry was centrifuged (1200g for 12 min). The fluid phase was passed through a 0.45-µm filter and then liquid-liquid extracted with Nanopure water and dichloromethane (DCM), partitioning the PAH into the DCM phase. Deuterated PAHs (same as above) were added to the DCM extracts to serve as internal standards. All gut fluid PAH concentrations were adjusted for the recovery of the deuterated PAH with the same number of rings. Typical recoveries were 52 ( 8% for 3-ring PAHs, 88 ( 8% for 4-ring PAHs, and 84 ( 10% for 5-ring PAHs. PAH Cleanup and Measurement. DCM extracts were purified in the dark by passage through sodium sulfate and ENVI-Florisil columns (Supelco Part No. 5-7058) to remove polar and sulfur compounds and dried under nitrogen gas at 38 °C. Silicic acid columns were substituted for Florisil columns when measuring total PAH. Dried samples were reconstituted in 1:1 acetonitrile:water (v/v), filtered through a 0.45-µm syringe filter, and injected into a Hitachi D-7000 high-pressure liquid chromatograph (HPLC). A Vydac 201 TP, 5 µm, 250 × 4.6 mm column was used under the following operational conditions: flow rate ) 1.0 mL min-1; temperature ) 29 °C; injection volume ) 250 µL; mobile phase ) 1:1 acetonitrile:water (v/v) for 5 min, ramping to 100:0 in 15

TABLE 1. Geochemical Characteristics of the Sediments Investigated

location Surface Area (m2 g-1) TOC (mg g-1) OC:SFA ratio (mg m-2) Total Sedimentary PAHsa (µg g-1) Phen Anthr Fluor Pyrene BaA Chrys BbF BkF BaP DB[ah] B[ghi]pe Ind[123] Σ PAH

Little Fort Mystic Independence, Pier B, log Channel, MA MA CA Kowb 15.4

3.7

18.5

71.7 4.7

28.1 7.6

12.8 0.7

120 18.2 146 74.2 37.6 50.9 36.2 16.8 43.0 2.5 24.4 18.2

7.0 1.3 16.0 11.0 4.4 6.4 5.0 2.4 6.1 0.1 3.9 3.2

12.0 27.3 135 310 27.2 109 71.3 36.0 71.2 11.9 25.6 16.1

588

66.7

852

4.55 4.55 5.12 5.11 5.70 5.70 6.20 6.20 6.11 6.69 6.70 6.65

a

Abbreviations: Phen, phenanthrene; Anthr, anthracene; Fluor, fluoranthene; BaA, benzo[a]anthracene; Chrys, chrysene; BbF, benzo[b]fluoranthene; BkF, benzo[k]fluoranthene; BaP, benzo[a]pyrene; DB[ah], dibenz[a,h]anthracene; B[ghi]pe, benzo[ghi]perylene; Ind[123], indeno[1,2,3-cd]pyrene. b Log Kow values from ref 34.

min, and holding for 8 min. PAHs were identified with a diode array UV detector, quantifying peaks at 254 nm. Using UV absorption, detection limits were approximately 0.001 µg (mL of gut fluid)-1 for individual PAHs.

Results Sediment Characteristics. Total and some individual PAH concentrations varied by as much as an order of magnitude among the sediments (Table 1), although all sites had high levels of total PAH contamination as compared to other harbors in the United States (25). Ft. Independence sediments had the coarsest grain size with a specific surface area (SFA) of 3.7 m2 g-1. OC:SFA ratios suggest that both Boston Harbor sediments were heavily loaded with anthropogenically derived organic material while Pier 8 had normal organic matter loading (21). Digestive Fluid Solubilization of PAHs. After incubations with sediment, 12 PAHs were quantified (Table 1). In this section, only representative PAHs are discussed, but similar results were obtained for the other PAHs unless noted. As potential sorption of PAHs during the initial filtration of gut fluids was not accounted for, reported values should be considered minimum PAH concentrations in gut fluids. Kinetics. For most PAHs from Little Mystic Channel sediment, except for pyrene and fluoranthene, the majority of PAH release from sediment to gut fluid occurred by the first sampling at 15 min (Figure 1). With longer incubations, only pyrene and fluoranthene concentrations increased significantly. Dilution of Gut Fluid. In experiments with pure PAHs, artificial seawater dissolved 0.34 µg of phenanthrene mL-1 and 3.5 × 10-3 µg of benzo[a]pyrene mL-1 (Figure 2)svalues similar to seawater solubilities previously reported (26, 27). Full-strength gut fluids solubilized much higher levels of phenanthrene (4.6 µg mL-1, approximately 10 times seawater solubility) and benzo[a]pyrene (2.0 µg mL-1, almost 1000 times seawater solubility). Benzo[a]pyrene concentrations in SDS (2.0 mM) and BSA (250 mM) solutions were 3.5 and 1.7 µg mL-1 respectively, similar to that in gut fluids.

FIGURE 1. Kinetics of PAH release into gut fluids. Plots of PAH release with time of incubation of Little Mystic Channel sediment. Each graph represents data for an individual PAH (SRT, stomach residence time; GRT, gut residence time for sediments passed through Arenicola marina). Error bars are (1 SD. Mixtures of gut fluid or SDS with seawater showed biphasic concentrations of PAHs (Figure 2A,C,D), which implies solubilization into micelles. Below the cmd, little PAH was dissolved, and there was a low response slope of PAH concentration to increasing proportion of gut fluid. In mixtures above the cmd, micelles formed and caused a more rapid increase in PAH solubilization with increasing proportion of gut fluid. For both gut fluid and SDS, PAH solubility increased at dilutions just below the cmd indicated by contact angle measurements. Solubilization of highly hydrophobic compounds by surfactant solutions just below the cmc can increase due to the formation of small (dimer, trimer, etc.) micellar forms (28, 29). In contrast, the relationship between BSA concentration and PAH dissolution was clearly not biphasic. Instead, PAH concentration increased linearly in response to additional BSA. Therefore BSA molecules do not exhibit aggregation behavior in the range of concentrations investigated, which influences PAH absorption. The relative importance of the micellar phase versus other gut fluid constituents in solubilizing PAHs was determined by fitting a logarithmic regression to PAH concentration data below the cmd and extrapolating to 100% gut fluid to determine solubilization by nonmicellar compounds in fullstrength gut fluids. These regressions (Figure 2C,D) imply that micelles are responsible for the majority of pure PAH solubilization in A. marina gut fluidss77% of the phenanthrene and 80% of the benzo[a]pyrene. Comparison of micellar solubilization of phenanthrene and benzo[a]pyrene requires normalization of PAH concentrations to the surfactant concentrations initially present in each gut fluid, as the gut fluid incubated with phenanthrene was collected at a different time than the fluid used with benzo[a]pyrene and all other experiments. Surfactant concentrations were not measured. However, if we assume that concentrations are equal at the cmd if surfactant composition in each fluid is the same, then regression of data points above the cmd yields the PAH solubilization per doubling of surfactant concentration above the cmc. This analysis yields phenanthrene solubilization of 1.28 µg of phenanthrene VOL. 34, NO. 7, 2000 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 2. Contact angles and pure PAH solubilization by sodium dodecyl sulfate (SDS) (A), bovine serum albumin (BSA) (B), and digestive fluids (C and D) solutions, each titrated with clean seawater. Abscissa represents the dilutions of the original solution. Left ordinate represents the contact angle (O). Right ordinate is the concentration of PAH solubilized (b). Thin solid lines fit to contact angle data intersect at the cmd. In panels C and D, thicker solid lines fit to PAH concentration data below the cmd are extrapolated to 100% gut fluid to determine PAH solubilization by nonmicellar components of the gut fluid. For both PAHs, logarithmic regression gives a tighter fit than a linear regression of the data. The nonmicellar compounds in Arenicola marina gut fluids solubilize 23% of the total phenanthrene and 20% of the total benzo[a]pyrene; thus, micelles are responsible for ∼80% of the PAH solubilized by 100% gut fluid. Error bars are (1 SD. doubling-1 as compared with 2.35 µg of benzo[a]pyrene doubling-1. Switching to molar concentrations, 7.20 nmol of phenanthrene doubling-1 and 9.30 nmol of benzo[a]pyrene doubling-1 were dissolved; thus, gut fluids solubilized very similar molar amounts of these two PAHs. As found with pure PAHs, release of some 3- and 4-ring sedimentary PAHs (e.g., pyrene from Pier 8 and phenanthrene from Little Mystic Channel) exhibited similar biphasic release trends indicative of surfactant micelle solubilization (Figure 3). For samples with clear biphasic plots, logarithmic regression of data below the cmd implies that micelles solubilized 50-60% of these PAHs at 100% gut fluid. However, many larger PAHs (e.g., benzo[a]pyrene from Pier 8 and Little Mystic Channel sediments) showed more continuous increases as gut fluid approached full-strength. Therefore, the role of digestive micelles in solubilizing certain PAHs appears reduced when incubated with sediment as compared to the pure PAH experiments. Solid-Fluid Ratio. At low (1 correspond to more PAH in gut fluid than predicted by EqP. As PAH hydrophobicity increases, EqP increasingly underestimates the amount of PAH released to gut fluids from each sediment. and other nonionic organic compounds is

Cd ) Cs/( foc(1.01Kow0.983)) Using measured total PAH concentrations, organic carbon contents, and reported Kow values (34), aqueous concentrations of PAHs in equilibrium with sediment can be calculated. Predicted equilibrium aqueous concentrations thus calculated can be compared to values of PAH released to gut fluid at a physiologically reasonable solid-fluid ratio (0.5 g mL-1; Figure 7). While this is a comparison of two different pools of PAHssfreely dissolved PAHs (Cd) and gut fluidsolubilized PAHssboth are bioavailable. Concentrations in gut fluid were generally much greater than predicted to be available by EqP theory, especially as PAH size increased. For example, the gut fluid concentration of benzo[ghi]perylene from Pier 8 was 126 times greater than the aqueous concentration predicted by EqP. The implication for bioavailability is that digestion results in enhanced exposure to all of the PAHs with log Kow > 5.5 but not all of the less hydrophobic PAHs as compared to the aqueous phase. Factors Influencing PAH Concentration in Gut Fluids. PAH release from sediments was generally in excess of that predicted by EqP theory (Figure 7), but it was considerably less than could be solubilized from pure PAH (Figure 2). We suggest two possible explanations for this shortfall. First, it appears that surfactants, which are responsible for a significant fraction of PAH solubilization, were adsorbed by sediment (Figure 5). Thus, fewer micelles likely remained after the sediment incubation to absorb PAH and hold them in solution. Surfactant adsorption was greatest in the Little Mystic Channel sediments, which had the highest organic matter loadings but not the highest sediment surface area. This result suggests that organic loading of sediments may reduce PAH bioavailability not only by providing more solid sorbant for PAH but also for the digestive agents that solubilize it. Previously, organic matter has been found to be both an important (30) and an unimportant (35) phase for commercial surfactant sorption to sediments. The presence of micelles also varies for physiological reasons. For example, micelles are most abundant in midsections of the gut (12) so that solubilization ought to be reduced (in extent and perhaps in rate) in foregut and hindgut compartments. Food quality can affect surfactant production;

for example, the polychaete Nereis virens increases surfactant production in response to sediment in its diet (20). Second, it is likely that other lipids can compete with PAH for space in digestive micelles. When present in close proximity, e.g., in a hydrophobic phase such as a micelle, mixtures of hydrophobic compounds can have a synergistic or antagonistic effect on each other’s solubility (36, 37). For example, when micelles solubilize mixtures of PAHs, larger PAHs tend to displace smaller PAHs from micelle cores, decreasing the overall solubility of the smaller compounds (14). Competitive interactions are not restricted to the same family of organic compounds (37, 38). A wide variety of potential competitors are present in these sediments; for example, Boston Harbor sediments have PCB concentrations roughly equal to PAH concentrations (39). Gut fluid concentrations of PAH do not simply increase in response to additional sediment contamination. PAH concentrations in gut fluids appear to reach a plateau (Figure 4), with saturation of the hydrophobic phase perhaps limiting the amount of PAH released to the gut fluid of one individual. This result is not due to the accessibility of PAHs in the sedimentary matrix; incubations at low solid-fluid ratios released larger percentages of PAHs than at saturation, and repeat incubations of the same sediment sample released additional PAHs to fresh gut fluid. Clearly, an animal’s physiology sets both upper and lower limits on the availability of contaminants transiting through its gut; thus, digestive bioavailability cannot be predicted with knowledge of sediment geochemistry alone.

Acknowledgments We thank L. Schick for helpful discussions concerning HPLC determination of PAH. Many University of Maine graduate students helped collect worms. The Office of Naval Research funded this work. This is contribution no. 348 from the Darling Marine Center.

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Received for review August 2, 1999. Revised manuscript received January 5, 2000. Accepted January 6, 2000. ES990885I