Environ. Sci. Technol. 2001, 35, 4060-4065
Marine Protozoa Produce Organic Matter with a High Affinity for PCBs during Grazing E L I Z A B E T H B . K U J A W I N S K I , †,‡,§ JOHN W. FARRINGTON,‡ AND J A M E S W . M O F F E T T * ,‡ Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543
Processes influencing organic carbon distribution and composition can control the speciation of organic contaminants such as polychlorinated biphenyls (PCBs) and ultimately determine their residence time in aquatic environments. Protozoan grazers are active in the remineralization and recycling of organic material both in the water column and at the sediment-water interface. Thus, they influence the quality and quantity of potential PCB binding substrates in the suspended and dissolved phases of aqueous systems. In this study, common headspace systems were used to compare the chlorobiphenylbinding affinity of dissolved organic carbon (DOC) in protozoan and bacterial culture filtrates (10 000 Da nominal size range (30-40% of total) was predominantly complex polysaccharide material. This material appeared to be biologically derived rather than the product of geopolymerization reactions (14, 15). Further culture studies by Aluwihare and Repeta (16) showed that phytoplankton exudates could be degraded by bacterial assemblages to material with similar spectral, and presumably structural, properties as marine high molecular weight DOC. If DOC is predominantly carbohydrate, it will have a relatively low C:O ratio and thus low affinity for hydrophobic compounds [shown for PAHs (17)]. Highly polar compounds (low C:O ratios) have been suggested to be less sorbent than nonpolar compounds (high C:O ratios) (1820). However, aggregates with nonpolar microenvironments can exhibit higher binding affinities than those predicted by chemical composition alone (21). Previous work has shown that nanozooplankton, or protozoa, are a potentially important source of dissolved and colloidal organic material in natural systems (22-27). Protozoa can affect the size spectrum and the composition of particulate material by ingesting bacteria and large colloids and excreting both dissolved and colloidal material [e.g., organic (22, 27); inorganic (28)]. Grazer-modified DOM is presumed to be derived from bacterial prey, but its exact chemical composition has not been ascertained. Nagata and Kirchman (23) observed colloidal phospholipid-rich material, while Tranvik (22) suggested that grazer-modified DOC was dominated by bacterial internal cellular components. Production of DOM by grazers is likely to be important for chlorobiphenyl (CB) speciation in carbon-rich systems with dense protozoan populations (29, 30). Studies by Baker et al. (31) and Sanders et al. (32) indicated increased remobilization of PCBs over that predicted by organic carbon remineralization at the sediment-water interface of two lake systems. Using these data, we propose that chemical and structural changes were occurring within the organic material at the sediment-water interface, which in turn affected the fate and transport of PCBs by altering the affinity of bulk DOC for PCBs. More specifically, DOC with high affinity for PCBs could have been sequestering them in the dissolved or suspended pools, thus retarding their burial in sediments. The microbial food web (protozoa and bacteria) has been shown to be efficient in remineralizing organic material (26, 33, 34), and it is possible that microbial-mediated processes were responsible for the preferential remobilization of PCBs by production of DOC with high affinity for PCBs. Protozoan grazers can also affect the fate and transport of organic contaminants by altering the chemical composition of sediment particle surfaces or by changing the population dynamics of the bacterial assemblage present. 10.1021/es001536n CCC: $20.00
2001 American Chemical Society Published on Web 09/11/2001
Surface-associated protozoa feed on bacteria living on the surface of sediment particles and excrete organic material that can associate with these surfaces (35). In addition, protozoa can indirectly affect the biodegradation of contaminants by altering the population dynamics of the bacteria responsible for the degradation. For example, high protozoan populations and high biodegradation rates were observed simultaneously in a jet fuel-contaminated site (29). The authors proposed that efficient grazing by protozoa forced the indigenous bacterial populations to grow exponentially with resultant high biodegradation rates (29). In this study, we focused on the hypothesis that protozoan grazers produce colloidal or dissolved organic matter with high affinity for PCBs. To that end, we ascertained the affinity of grazer-modified DOC for PCBs relative to bacterial-derived and seawater DOC. Cultures of three marine protozoan grazers and a bacterial control were filtered to remove cells and large organic material (>0.2 µm). The affinity of the remaining material (
