Environ. Sci. Technol. 2006, 40, 2586-2593
On the Relative Significance of Bacteria for the Distribution of Polychlorinated Biphenyls in Arctic Ocean Surface Waters A N N A S O B E K , * ,†,‡ K A L L E O L L I , § A N D O ¨ RJAN GUSTAFSSON† Department of Applied Environmental Science, Stockholm University, SE-10691 Stockholm, Sweden, Agroscope FAL Reckenholz, Swiss Federal Research Station for Agroecology and Agriculture, Reckenholzstrasse 191, CH-8046 Zu ¨ rich, Switzerland, and Institute of Botany and Ecology, University of Tartu, Lai st 40, 51005, Tartu, Estonia
This study presents the first field observations of polychlorinated biphenyls (PCB) in bacteria in oceanic waters. To contribute to the limited knowledge of what role bacteria play in the dynamics of hydrophobic organic contaminants (HOCs) in surface seawater, PCB concentrations were measured in bacteria (0.2-2 µm) collected at seven stations in the northern Barents Sea marginal ice zone (MIZ) and the central Arctic Ocean. Concentrations of individual PCB congeners in bacteria were 0.5-5 ng/g oc (organic carbon), which was as high as or higher than PCB concentrations in bulk particulate organic carbon (POC, “phytoplankton”; >0.7 µm). Considering the relative biomasses of phytoplankton and bacteria, the amount of PCB in bacteria was generally 5-20% of that in phytoplankton, but at two stations the bacterial biomass contained more PCBs than the phytoplankton pool. This study further showed that efficient PCB uptake in bacteria may be described by an apparent equilibrium partitioning model with linear regressions between the organic-carbonnormalized partition coefficient and the octanol-water partition coefficient (log Kbact-oc-log Kow).
Introduction Hydrophobic organic contaminants (HOCs) such as polychlorinated biphenyls (PCBs) are widely distributed in the environment, cause toxic effects to biota, and bioaccumulate in food webs, e.g., refs 1-3. The distribution of HOCs in marine waters is believed to be largely governed by partitioning to biogenic particulate organic carbon (POC). While partitioning and uptake of HOCs in phytoplankton and zooplankton has been widely studied, e.g., refs 4-9, information on HOC association with marine bacteria, found in abundances of 104 to 5 × 106 cells/mL (10), is sorely missing. This group of micrometer-sized cells may contribute significantly to the carbon pool in the marine water column, and it has been shown that bacterial biomass may even exceed that of phytoplankton in oligotrophic marine waters (11). HOC concentrations in field-sampled marine bacteria have * Corresponding author phone: +41 44 377 7596; fax: +41 44 377 72 01; e-mail:
[email protected]. † Stockholm University. ‡ Swiss Federal Research Station for Agroecology and Agriculture. § University of Tartu. 2586
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only been reported on three occasions in the brackish Baltic Sea (8, 12), indicating that PCBs sorb well to Baltic Sea bacteria, with organic-carbon-normalized concentrations of the same level as that found in phytoplankton for any given PCB congener. A recent study in Lake Superior confirmed that freshwater bacteria may also contain PCBs at similar or even higher levels than in bulk POC (13). Sorption of HOCs to bacteria may influence a broad set of HOC fate processes, including residence and thus exposure times to surface ocean ecosystem, and bioaccumulation in the marine food web. Since bacterial cells do not have a settling velocity relative typical surface ocean mixing velocities, its organic carbon is to a large extent recirculated by bacterivore grazing and viral lysis (e.g., refs 14, 15). Significant sorption of HOCs to bacteria may contribute to longer residence times of these contaminants in the recycling environment by reducing the degree of settling export and burial of HOCs in underlying sediments. In the microbial heterotrophic food web (the microbial loop), phytoplankton exudates (originating from photosynthesis) are utilized for bacterial biomass. Bacteria, in turn, are grazed upon by heterotrophic flagellates, ciliates, and protozoa, which are grazed by zooplankton. In oligotrophic plankton systems, heterotrophs have a dominant functional role in terms of carbon and nutrient flows (16). There is thus a potential for the microbial loop to significantly transfer HOCs into the base of the pelagic food web, which also has been proposed from laboratory studies of trophic transfer of PCB 153 (17, 18). The main objective of the present study was to contribute to the limited knowledge of what role bacteria play in the dynamics of HOCs in surface seawater. Ambient trace-level concentrations of PCBs were measured in bacterial samples (0.2-2 µm) obtained in the northern Barents Sea marginal ice zone (MIZ) and the central Arctic Ocean, thus reflecting long-range transport processes of HOCs to these remote regions. The bacterial fraction was collected with a highcapacity all stainless steel/ceramics cross-flow filtration (CFF) system able to process the large water volumes (>3000 L/sample) that are necessary for quantification of ambient PCB levels.
Materials and Methods Sampling for PCBs. Surface seawater samples were collected onboard the icebreaker ODEN during the Swedish Arctic Ocean expedition (SWEDARCTIC 2001) between June and August 2001. Five sampling stations were situated in the marginal ice zone (MIZ) in the northern Barents Sea, one station in the Makarov Basin east of the Lomonosov ridge at 88°N (Canadian Basin), and one station in the North Pole area on the Eurasian Basin side at 89°N (Figure 1, Table 1). A stainless steel seawater-intake system situated at the prow of the ship at a water depth of approximately 8 m was used to continuously sample PCBs online. The approximate total flow through the seawater intake system was 50 L/min. A detailed description of the seawater intake, the shipboard laboratory, and the clean sample handling is available (19, 20). The procedures for collecting particle-associated and dissolved PCBs using GF/F filters and polyurethane adsorbents are described in a previous study (21). The high-throughput cross-flow filtration (CFF) system used to isolate the bacterial fraction (0.2-2 µm) for PCB analysis is similar to the system used in the previous Baltic expeditions by Broman and co-workers (12). To minimize the risk of organic contamination and sorptive losses of the hydrophobic PCBs to wetted surfaces, this Millipore Ceraflo 10.1021/es0524907 CCC: $33.50
2006 American Chemical Society Published on Web 03/16/2006
FIGURE 1. Sampling locations in the northern Barents Sea MIZ and the central Arctic Ocean. Maximum and minimum ice extents represent a multiyear average position (3). The ice situation at sampling of each station is listed in Table 1. CFF system was constructed entirely in stainless steel with the tubular CFF filter elements made of inert Al2O3. Nine new 836 mm long tubular ceramic-filter elements each with a surface area of 0.14 m2 and cutoff of 0.2 µm (Vivendi Water Systems AB, Stockholm, Sweden) were loaded into the Ceraflo housing. While the filter passing permeate is discarded, the retained >0.2 µm solution is recycled into the stainless steel retentate container, where it is combined with a permeatecompensating inflow of feedwater, and again passed by the CFF filter. In CFF, formation of artifactual filtration cakes is avoided as the filters are “self-cleaned” by the continuously repeated tangential flow of the increasingly concentrated retentate solution, e.g., ref 22. A transmembrane pressure of about 2 bar resulted in a permeate flow of about 6 L/min. The tubing directing water from the seawater intake into the CFF system was made of silicone, and all gaskets were made of either silicone or Teflon. A prefilter (Millipore CP20, 2 µm capsule) was placed before the CFF system to obtain an operational bacterial fraction of 0.2-2 µm. The final retentate samples, consisting of approximately 3-10 L of concentrated bacteria suspension (concentration factors 400-1900; total
processed water volumes of 3-20 m3), were collected in precleaned glass bottles containing a cocktail of chloramphenicol (5 mg/L), tetracycline (5 mg/L), HgCl2 (10 mg/L), and NaN3 (325 mg/L) to minimize bacterial activity. The sample-containing bottles were placed in the dark at 4 °C. Each sample was centrifuged at 18000g and subsampled for analysis of particulate organic carbon (POC), and the remaining pellets were stored at -18 °C until PCB analysis. Bacterial Enumeration and Production. Aliquots for bacterial counts (20 mL) were subsampled from 10 L Niskin bottles attached to the CTD rosette (see below) representing fixed depths between the surface water and 200 m. Aliquots were preserved immediately with glutaraldehyde (2.5% final concentration) and were within 1-5 days filtered onto black Poretics (0.2 µm pore size) membrane filters, stained with DAPI (23), and stored at -22 °C until analysis by a Leica DBRB epifluorescence microscope (UV excitation light, 100× oil immersion objective). The size and shape of the bacteria was calculated assuming an ellipsoidal shape of the cells. Bacterial cell volume was converted to carbon using a conservative conversion factor of 0.22 pg C /µm3 (24). For the MIZ samples, where no cell size was available, a cell carbon content of 20 fg (25) was used instead. Bacterial production was measured using the microcentrifuge radiolabeled leucine incorporation technique (26) using a conversion factor of 3.1 kg C/mol leucine incorporated (27). Sampling of Ancillary Biogeochemical and Ecological Parameters. Salinity and temperature were continuously measured and logged by a thermosalinograph (Hydrolab, Austin, TX) coupled to the seawater intake system at 8 m depth. The procedures for sampling and analysis of humic substances (HS), total organic carbon (TOC), POC, primary production, and nutrient concentrations have been described elsewhere (21, 28, 29) and are described here only briefly. At the onset of each sampling occasion a full CTD profile was obtained to determine the depth of the mixed layer. Water for analysis of HS, TOC, transparent exopolymer particles (TEP), and nutrients was collected from 10 m depth with Niskin bottles connected to the conductivity-temperaturedepth (CTD) rosette. Fluorescence-based determination of HS content was performed following Wedborg et al. (30) and normalized to quinine sulfate equivalents (µg QSE/L). A spectrophotometric method was employed to determine TEP concentrations in the water (31), normalizing to a standard curve of gum xanthan (µg GXE/L). Mineral nutrients (NO2, NO3, PO4, SiO4) were taken into 20 mL plastic scintillation vials, preserved with a drop of chloroform, and analyzed on
TABLE 1. Hydrological and Biogeochemical Characteristics of the Sampling Sites (MIZ ) Marginal Ice Zone) latitude (°N) longitude (°E) MYIa (%) salinity T (°C) HSc (µg QSE/L) TEPd (µgGXE/L) TOC (mg/L) POC (µg/L) bact-oc (µg/L) prim prode (mg C/m2 day) nitrate (µM) phosphate (µM) silicate (µM)
MIZ A
MIZ B
MIZ C
MIZ D
MIZ E
89°Ν
Makarov
77.49-77.54 29.53-29.38 0.05) of the log KPOC-log Kow correlation, supporting that the degree of partitioning was not affected by phytoplankton growth rates (7). The slopes were not correlated with TEP concentrations either (slope vs TEP, r2 ) 0.33, p > 0.05). Comparison of PCB Concentrations in Bacteria and POC. The ratio of PCB concentrations in bulk POC (“phytoplankton”; >0.7 µm) and bacterial organic carbon (bactoc) was plotted as a function of log Kow (Figure 3). Some of the scatter observed in Figure 3 may be attributed to VOL. 40, NO. 8, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. log Kbact-oc as a function of log Kow (49). The dotted lines represent a 1:1 relationship and serve as a common reference for the different stations. propagated analytical uncertainties; therefore, only general trends are evaluated here. At stations MIZ A, MIZ B, and MIZ D (Figure 3A-C), PCB concentrations in POC and bact-oc were within a factor of 2, irrespective of PCB hydrophobicity. At stations MIZ C and Makarov (Figure 3D,E), PCB concentrations were higher in the bact-oc fraction for all congeners by factors of 2-10. At stations MIZ E and 89°N (Figure 3F,G), the ratio between PCB concentrations in POC and bact-oc increased with hydrophobicity from 0.5 for tetrachlorinated to 2 for hepta- and octachlorinated congeners. An increasing trend with hydrophobicity was also observed for MIZ C (Figure 3D). The only uptake route for PCBs into phytoplankton and bacteria is passive partitioning with surrounding water. Nonequilibrium partitioning results thereby in lower contamination loads in the organic phase than at equilibrium. However, since both bacteria and phytoplankton were apparently in near-equilibrium with the surrounding seawater, the remaining factor affecting PCB loads in the 2590
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two phases is the ability of the organic matter to dissolve PCBs. Stations MIZ A, B, and D had similar slopes for bacteria and phytoplankton and were the stations with CPOC/Cbact-oc ratios closest to one, independent of log Kow (Figure 3A-C). The sorptive behavior toward PCBs of bacteria and phytoplankton biomasses was thus similar at these stations. The hydrophobicity dependence at stations MIZ C, MIZ E, and 89°N reflects the higher slope for the POC fraction at these stations, relative to bact-oc. Within the broad biogeochemical framework sampled for this study, no single parameter could explain the sorptive behavior of POC and bact-oc at the different stations. The TEP data provides a measure of exudated carbon from phytoplankton, which may be used by bacteria as energy. Partitioning of PCBs to bact-oc relative to POC was the highest at stations MIZ C and Makarov (Figure 3D,E), which were the stations that displayed the lowest TEP concentrations together with the 89°N station (Table 1). Perhaps high TEP concentrations in the surface water may
FIGURE 3. Ratio of PCB concentrations in POC (“phytoplankton”; >0.7 µm) and bact-oc as a function of log Kow (49). Concentration data for the >0.7 µm fraction are from ref 21. affect the sorptive behavior of bacteria given that the use of TEP as an energy source for bacteria results in a composition of the organic matter that is different relative to the use of other energy sources. The effect of utilization of different energy sources on the sorptive behavior of bacterial biomass is however an unstudied area, and more research is needed before any potential mechanisms can be presented. Humic substances (Table 1), which are also used by bacteria (47), did not correlate to the degree of partitioning of PCBs between water and bacteria (slope vs HS, r2 ) 0.23, p > 0.05). Overall, these results show that Arctic surface seawater bacteria have a sorptive behavior toward HOCs similar to that of phytoplankton (Figure 3). Bacteria may therefore constitute a significant reservoir for HOCs in the marine water column, considering that bacterial biomass in oligotrophic marine waters may exceed phytoplankton biomass (11). In the present study, bacterial biomass was generally a factor of 10 lower than POC (Table 1), using a conservative volumeto-carbon conversion factor (see Materials and Methods section). The amount of PCB in the bacterial fraction was therefore generally 5-20% of the PCB load in the POC
(“phytoplankton"; >0.7 µm) isolate at 10 m depth. However, for most congeners at stations MIZ C and Makarov, the PCB load was a factor of 2 higher in the bacterial pool than in the phytoplankton size fraction. Hence, although the conclusions drawn here are based on data from only seven stations in the Arctic Ocean, the results indicate that the phytoplankton carbon pool generally carries a higher load of HOCs than bacteria. Under certain circumstances the bacterial carbon pool may however contain more HOCs than phytoplankton. Importance of Bacteria in Trophic Transfer of HOCs. Some previous laboratory-based studies have highlighted the potential importance of bacteria and the microbial heterotrophic food web in trophic transfer of HOCs (17, 18), and a need for incorporating bacteria in food web modeling was suggested recently (13). A prerequisite for this hypothesis is however that the ingestive uptake is more effective in assimilating PCBs than exchange with water for heterotrophic plankton consuming bacteria and phytoplankton. Hence, even in oligotrophic systems in which the microbial heterotrophic food web is important in terms of carbon flux, bacteria may prove insignificant in the trophic transfer of VOL. 40, NO. 8, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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HOCs if the heterotrophic organisms consuming bacteria mainly assimilate HOCs from the water. Kujawinski et al. (48) have shown in laboratory experiments that uptake through food ingestion in protozoa was insignificant compared to equilibrium partitioning. Further, uptake of PCBs in zooplankton in a previous study in the Arctic Ocean was shown to be dominated by passive partitioning and not biomagnification (21). Hence, while the present study shows that PCB concentrations in bacteria are as high or higher than in POC (“phytoplankton”), this apparently does not significantly influence PCB concentrations higher up in the food web, which is in contrast to the recent postulate by Hudson et al. (13). The limited number of available field studies on PCB concentrations in bacteria and other parts of the microbial loop highlight the need for more work to evaluate the importance of the heterotrophic microbial food web in biomagnification of PCBs in marine food webs.
Acknowledgments We thank Kerstin Grunder and Zofia Kukulska for analytical work and Ralf Dahlqvist for providing the map. Lars Tranvik and Johan Knulst are gratefully thanked for contributing data on bacterial production, size, and numbers. We also thank captain and crew on the icebreaker ODEN and the Swedish Polar Secretariat (SWEDARCTIC 2001) as well as helpful colleagues in the field. This work was financially supported by the EU DG XII (FAMIZ EVK-CT-2000-00024) and the Swedish Research Council (VR Grant 21.0/2002-0629). The Stockholm Marine Research Centre (SMF) is acknowledged for a Ph.D. stipend to Anna Sobek and the Swedish Research Council for a senior research fellowship to O ¨ rjan Gustafsson (VR Grant 629-2002-2309).
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Received for review December 13, 2005. Revised manuscript received February 21, 2006. Accepted February 22, 2006. ES0524907
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