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Effects of Four Aromatic Organic Pollutants on Microbial Glucose Metabolism and Thymidine Incorporation in Marine Sedimentst JAMES E

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Effects of Four Aromatic Organic Pollutants on Microbial Glucose Metabolism and Thymidine Incorporation in Marine Sedimentst JAMES E APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Apr. 1985, p. 828-835 Vol. 49, No. 4 0099-2240/85/040828-08$02.OO/0 Copyright C 1985, American Society for Microbiology Effects of Four Aromatic Organic Pollutants on Microbial Glucose Metabolism and Thymidine Incorporation in Marine Sedimentst JAMES E. BAUER AND DOUGLAS G. CAPONE* Marine Sciences Research Center, State University of New York, Stony Brook, New York 11794 Received 18 October 1984/Accepted 21 January 1985 The metabolism of D-[U-14C]glucose and the incorporation of [methyl-3H]thymidine by aerobic and anaerobic marine sediment microbes exposed to 1 to 1,000 ppm anthracene, naphthalene, p,p'-dichlorodiphenyltri- chloroethane, and pentachlorophenol were examined. Cell-specific rates of [14C]glucose metabolism averaged 1.7 x 10-21 and 0.5 x 10-21 mol/min per cell for aerobic and anaerobic sediment slurries, respectively; [3Hlthymidine incorporation rates averaged 43 x 10-24 and 9 x 10-24 mol/min per cell for aerobic and anaerobic slurries, respectively. Aerobic sediments exposed to three of the organic pollutants for 2 to 7 days showed recovery of both activities. Anaerobic sediments showed little recovery after 2 days of pre-exposure to the pollutants. We conclude that (i) anaerobic sediments are more sensitive than aerobic sediments to pollutant additions; (ii) [3HJthymidine incorporation is more sensitive to pollutant additions than is [14C]glucose metabolism; and (iii) the toxicity of the pollutants increased in the following order: anthracene, p,p'- dichlorodiphenyltrichloroethane, naphthalene, and pentachlorophenol. Coastal marine sediments, which are sites of intensive and Sediments for aerobic studies were obtained by scraping important microbial activities (8), accumulate organic pollut- the top 0 to 2 mm of sediment with a sterile spatula and ants (2, 4, 16). The effects of organic pollutants on the placing the sample in a sterile glass beaker. Sediment for sediment biota, although possibly substantial, generally have anaerobic studies was collected from depths of 5 to 10 cm not been considered. Several studies have examined the and maintained anoxically until return to the Marine Sci- acute and chronic effects of complex organic mixtures such ences Research Center, within 1 h from the time of collec- as fuel oils (10, 11, 14) on organic carbon metabolism by tion. Flax Pond seawater, with a salinity of about 28 parts sedimentary microorganisms. A few studies have considered per thousand, was obtained from Flax Pond laboratory the alteration of activities in marine sediments as a result of where it had undergone coarse (10 ,um) filtration through individual pollutants (5, 18; J. Slater and D. G. Capone, in I. nylon cartridge filters. Duedall, ed., Wastes in the Ocean, vol. 9: Proceedings of Sediment subsamples were diluted 1:100 (volume the Fourth Ocean Disposal Symposium, in press). sediment:volume seawater) in filtered seawater (0.45-R,m, In the present investigation, we assessed the effects of type GA-6; Gelman Sciences, Inc., Ann Arbor, Mich.) and four aromatic organic pollutants, anthracene, naphthalene, kept well mixed on a magnetic stirrer while slurry was p,p'-dichlorodiphenyltrichloroethane (DDT), and pentachlo- dispensed. For anoxic sediments, all diluent seawater was rophenol (PCP), on two microbial activities common to both purged of oxygen by bubbling with nitrogen gas for at least oxic and anoxic coastal marine sediments. Anthracene and 30 min before dilution. All vessels containing anoxic slurries naphthalene are polycyclic aromatic hydrocarbons, whereas were immediately stoppered (butyl rubber stoppers; Thomas DDT and PCP are representative chlorinated aromatic pol- Scientific Co., Philadelphia, Pa.) after they were dispensed, lutants. The activities chosen for study were D-[U- and the headspace was purged with nitrogen gas for 1 min. 14C]glucose metabolism and [methyl-3H]thymidine ([3H]TdR) All experimental slurries were maintained at 25°C in the dark incorporation. The study allows comparison of the sensitiv- in temperature-controlled water baths with rotary shaking to ity of [3H]TdR incorporation relative to [14C]glucose metab- ensure rapid equilibration between the gas and liquid phases olism in toxicity studies involving sedimentary systems, and dispersal of pollutants. comparison of the sensitivity of aerobic and anaerobic Pollutant effects studies. The effects of anthracene, naph- marine sediments to pollutants, and assessment of the rela- thalene (Eastman Kodak Co., Rochester, N.Y.), DDT tive toxicity of the four pollutant compounds tested. (R.F.R. Corp., Hope, R.I.), and PCP (Aldrich Chemical Co., Milwaukee, Wis.) on D-[U-_4C]glucose metabolism and MATERIALS AND METHODS [3H]TdR incorporation were examined in short-term acute Sampling and sample preparation. Sediments for all labo- and longer term experiments. All comparisons of rates of ratory studies were obtained from an intertidal mudflat of activities among treatments were analyzed by single classi- Flax Pond Saltmarsh, Old Field, N.Y. The mud consisted of fication analysis of variance (23). Significance levels were set a fine organic-mineral mixture (3 to 7% loss on ignition) at the at P < 0.05 for all analyses. sediment-water interface which became more mineral-rich at In acute pollutant effects 5 ml depths of 5 to 10 cm. The depth of the oxidized surface layer studies, of diluted sediment varied seasonally from approximately 1 to 3 mm in summer slurry was transferred from batch preparations to 20 ml of to as much as 3 cm in winter. acid-washed borosilicate scintillation vials (Wheaton Indus- tries, Millville, N. J.). Controls received 5 Rl of pure acetone carrier. It was found in preliminary experiments that this volume of acetone did not alter significantly either [3H]TdR * Corresponding author. incorporation or [14C]glucose metabolism compared with t Contribution no. 467 of the Marine Sciences Research Center. samples that received no acetone. Pollutants were added to 828 VOL. 49, 1985 ORGANIC POLLUTANT EFFECTS ON SEDIMENTARY MICROBIOTA 829 treatment slurries in 5-,l acetone solutions; final concentra- filters with their light coating of collected sediment were tions ranged from 1 to 1,000 ppm (micrograms of pollutant removed and placed in 20-ml scintillation vials. Ethyl acetate per milliliter of slurry). Samples were shaken continuously (1 ml) was added to dissolve the filters, after which Protosol and incubated for 1 to 2 h before activity assays were tissue digester (1 ml; New England Nuclear Corp., Boston, performed. In addition, subsamples were taken for the Mass.) was also added. Vials were then capped, and diges- estimation of total bacterial numbers (20) and determination tion proceeded overnight at 25 to 30°C. The next day, 10 ml of cell-specific activity rates. of Econofluor scintillation cocktail (New England Nuclear) The effects of longer term exposures of the four pollutants was added to each vial. Samples were thoroughly shaken, on oxic ["'Ciglucose assimilation were assessed by preparing and the light floc was allowed to settle. large batch slurries (ca. 600 ml) of diluted sediment and The radioactivity in each sample was quantified by count- dispensing 100 ml into 125- or 250-ml Erlenmeyer flasks. ing in a Packard Tri-Carb scintillation counter. Quench Individual flasks then received 100 ,ul of acetone or organic curves were constructed by the external standards method. stock solutions containing one of the four pollutants (100 Counting efficiency was relatively low (8 to 10%) in these ppm final concentration). Triplicate subsamples were taken samples because of color quenching which could not be from each flask and assayed for ["'C]glucose metabolism in removed by 10% benzoyl peroxide oxidation. scintillation vials at selected intervals over a 7-day period. To ensure that all single time point measurements of Single flasks were deemed suitable for each experimental [3H]TdR incorporation were representative of linear uptake level on the basis of preliminary results, from which no kinetics, periodic time series of incorporation were per- significant differences among subsamples from replicate formed. Both oxic and anoxic incorporation were linear for flasks (receiving no treatment) with respect to total at least 60 min (data not shown). Generally, oxic experi- ["'C]glucose metabolism or percent respired to 1'CO2 or ments were conducted for 30 to 45 min, whereas anoxic [3H]TdR incorporation were found. experiments never exceeded 60 min. To investigate possible acclimation of microbial popula- ["'C]glucose metabolism assays. The format for assaying tions to pollutants through previous exposure, as well as the the metabolism of [14C]glucose was similar to that described effects of additional inputs on activities, 100-ml batch slur- above for the [3H]TdR assays. An autoclaved filtered seawa- ries were prepared as described above and dosed with 1 to ter solution (10 ,ul) of 5 ,uCi of (18.0 mCi mmoI-1) D-[U- 1,000 ppm of the pollutants or acetone. After 2 days, 14C]glucose (New England Nuclear) per ml was added to triplicate 5-ml subsamples of both control and pretreated each 5-ml sediment slurry subsample through the stopper batches were dispensed into scintillation vials. Initial con- with a microliter syringe. The final amount of glucose to be trols then received either S RI of acetone (control) or organic added was determined by a preliminary study which as- pollutant stock to the same level as the parallel pretreated sessed the kinetics of uptake, as suggested by Griffiths et al. samples (dosed, no pretreatment). Pretreated batch (13). Glucose uptake appeared to be saturated at glucose subsamples received either 5 1±l of acetone (pretreatment concentrations of about 100 pug/liter of slurry, and this control) or an additional quantity of organic pollutant iden- concentration was used in all subsequent incubations. In tical to the pretreatment concentration (pretreatment plus preliminary experiments, uptake of [14C]glucose (100 pig/liter retreatment). of slurry) by oxic sediment slurries (5 ml) remained linear for [3HJTdR incorporation. The incorporation of [3H]TdR to at least 60 min.
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