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The Effect of Bioremediation on the Microbial Populations of Oiled

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The Effect of Bioremediation on the Microbial Populations of Oiled THE EFFECT OF BIOREMEDIATION ON THE MICROBIAL POPULATIONS OF OILED BEACHES IN PRINCE WILLIAM SOUND, ALASKA Downloaded from http://meridian.allenpress.com/iosc/article-pdf/1993/1/469/2357220/2169-3358-1993-1-469.pdf by guest on 25 September 2021 Roger C. Prince, Richard E. Bare, Graham N. George, Copper E. Haith, Matthew J. Grossman, James R. Lute, David L. Elmendorf, Vera Minak-Bernero, James D. Senius, Lois G. Keim, Russell R. Chianelli, Stephen M. Hinton Exxon Research and Engineering Company Annandale, New Jersey 08801 Andrew R. Teal Imperial Oil Box 1020 Edmonton, Alberta T5J 2Ml, Canada ABSTRACT: Bioremediation, the stimulation of the natural process of likely limiting nutrients are nitrogen and phosphorus; so the bio- biodégradation, played an important role in the cleanup of the oil spill remediation strategy was to supply these nutrients in the form of from the Exxon Valdez in Prince William Sound, Alaska. Since there carefully chosen fertilizers.14,25,27 The success of this strategy was were already substantial indigenous populations of oil-degrading mi- assessed in several intensely monitored test sites by microbiological, crobes in the area, it was apparent that degradation was likely to be ecological, and chemical techniques.8,22,26,27 Here we report the results nutrient—notmicrobial—limited. Bioremediation therefore involved the of microbiological measurements in a survey that extended throughout application of carefully selected fertilizers to provide assimilable nitro- Prince William Sound and the Gulf of Alaska,19 and show that the gen and phosphorus to the indigenous organisms, with the intent to bioremediation strategy was successful at increasing the number of stimulate their activity and enhance their numbers. We show here that heterotrophic and oil-degrading bacteria in the beach sediments. We the indigenous microbial populations were indeed substantially in- also report the initial results of a taxonomic study aimed at identifying creased, throughout the sound, approximately one month after wide- the bacteria present in this environment. Our results also indicate that spread fertilizer applications in both 1989 and 1990. Furthermore, while the structure of the microbial ecosystem was returning to pre-spill oil-degrading bacteria made up a significant fraction of the microbial conditions by the summer of 1990, just one year after the spill. populations on contaminated beaches in September and October 1989, they had declined to less than 1 percent by the summer of 1990, suggest- ing that the microbial populations on the shorelines were returning to their pre-spill conditions. Methods The samples analyzed here were collected as part of an extensive monitoring of 27 sites beginning in September 1989, after cleanup operations were suspended because of winter weather, and ending The grounding of the Exxon Valdez on Bligh Reef on March 24, September 1990. Seventeen of the sites were within Prince William 1989, released approximately 11 million gallons (U.S.) of North Slope Sound and 10 in the Gulf of Alaska (Figure 1, Table 1). They were crude oil into the waters of Prince William Sound. A major storm a few chosen to cover the range of wave exposures (high, medium, and low days later spread the oil onto the shores of numerous small islands in energy shorelines) and to include areas that received washing alone, the western part of the sound, and out into the Gulf of Alaska. The washing plus bioremediation (fertilizer), bioremediation alone, and no subsequent cleanup washed much of the oil back to the water so that it treatment.19 All sampling sites had been oiled by the spill; no samples could be removed by skimmers. This was followed by the application of were collected from the unaffected parts of the sound. (Less than 15 fertilizers to the shorelines to stimulate the biodégradation of the percent of the shoreline was affected by the spill.) Samples were remaining oil by indigenous microbial populations.1416'23,25,27 collected from the surface and subsurface (10 to 20 cm) of upper, The logic of applying fertilizer as the bioremediation strategy was middle, and lower intertidal zones, and shipped to New Jersey on ice, that under pre-spill conditions the number of oil-degrading bacteria but not frozen, for analysis. was limited by the availability of oil as a carbon source. Prince William The indigenous microbes were washed off the sediment, and oil- Sound and the Gulf of Alaska have particularly abundant and diverse degrading and heterotrophic bacterial populations assessed by most- populations of oil-degrading bacteria, which have been attributed to probable-number techniques. Oil-degrading microbes were assessed the presence of natural marine oil seeps and terrestrial input of hydro- by the "sheen-screen" method,9 and the general heterotrophic popula- carbons from the conifers of the temperate rain forest.13 Nevertheless, tion, presumably including the oil-degrading population, was assessed the background level of hydrocarbons and hydrocarbon-degrading by growth on a nutrient marine broth in a similar fashion.22 The oil we bacteria in this environment is low. After the spill, oil-degrading bacteria used in the sheen-screen tests had been heated to 521° F to remove the were no longer limited by the availability of oil, and their numbers volatile components that would have evaporated from the spilled oil increased dramatically until they were limited by other factors. prior to its arrival at the shoreline. Twenty grams of sediment were In the highly porous aerobic sediments typical of this area, the most shaken in 80 mL of saline Bushnell-Haas medium11 for 20 minutes at 469 470 1993 OIL SPILL CONFERENCE Storey Is. ¿¿\£p Peak ls- Downloaded from http://meridian.allenpress.com/iosc/article-pdf/1993/1/469/2357220/2169-3358-1993-1-469.pdf by guest on 25 September 2021 60 30 h 60°15 Montague Island Initial Oiling B Heavy A, Moderate =^ r-60°N 20 I Location Map of Prince William Sound Figure 1. Location of the sampling sites in Prince William Sound, Alaska—the indicated extent of oil loading reflects the initial oiling in 1989; the area was essentially free of oil by 1992. 100 rpm prior to sequential dilution in 24-well plates. The plates were populations shown in Figure 2 vary over 7 orders of magnitude.) The incubated at 15° C for 7 (heterotrophic) or 14 (sheen-screen) days. large number of samples necessitated only a few being measured in Experiments using higher ionic strength and/or dilute surfactants triplicate; these showed excellent reproducibility, indicating that the gave no higher estimate of the numbers of organisms. Samples from tremendous range shown in Figure 2 reflects the true heterogeneity of the different beaches had different sediment sizes, but we estimate that the bacterial populations. the maximal difference in surface area would amount to less than 2 Preliminary identification of microbial isolates was made using clas- orders of magnitude difference. (Note that the estimates of microbial sical morphological criteria, and the Biolog identification system.7 BIOREMEDIATION 471 Table 1. Sampling sites samples represent a particularly challenging matrix for enumeration, since many of the organisms are intimately associated with the oil, which itself adheres to the sediment. To assess the efficacy of bio- Site Oiling^wave energy Treatment2 remediation from a microbiological perspective, we have focused on determining the total number of heterotrophic microorganisms (ones Prince William Sound that require complex organic substances for growth) and the number of N.E. Smith Is. Heavy oil/high FF/HP/BR these that are capable of growth on weathered crude oil. The methods 18 energy we have used, three-tube most-probable-number techniques, al- N.W. Smith Is. Heavy oil/high FF/HP lowed us to process the large number of samples collected in our surveys in a timely fashion. While the numbers quoted here may energy 18 N.E. Little Smith Is. Heavy oil/high BR represent a systematic underestimate of the true populations, the energy comparison of the populations on the fertilized and unfertilized Foul Passage Heavy oil/low energy FF/HP/BR* beaches, rather than their absolute numbers, is most germane here. Passage Point Heavy oil/moderate FF/HP/BR Figure 2 shows the frequency distributions of the microbial popula- energy tions on fertilized and unfertilized beaches in Prince William Sound, Downloaded from http://meridian.allenpress.com/iosc/article-pdf/1993/1/469/2357220/2169-3358-1993-1-469.pdf by guest on 25 September 2021 E. Herring Bay Heavy oil/low energy set aside while Figure 3 presents the median populations of oil-degrading and E. Green Is. Heavy oil/moderate BR heterotrophic bacteria in these samples, together with the ratio of energy these medians. The data include all tidal zones and both surface and W. Green Is. Heavy oil/high FF/HP/BR subsurface samples. Those shorelines that received fertilizer were energy treated (arrows in Figure 3) prior to the first sampling (August and Point Helen MR/FF/HP/BR early September 1989) and after the sampling in June 1990. Statistical Heavy oil/high 32 energy analysis using the nonparametric Mann-Whitney test indicates that N.E. Latouche Is. Heavy oil/high set aside the populations of both oil-degrading and heterotrophic bacteria were energy greater in samples collected from fertilized shorelines than in those N.E. Latouche Is. Heavy oil/high MR/FF/HP/BR from unfertilized areas, in both September 1989 and September 1990 energy (p < 0.05). Bioremediation increased the populations of both oil- Sleepy Bay Heavy oil/high MR/HP/BR degrading and heterotrophic microbes approximately 10- to 100-fold. energy This effect was not, however, seen beyond the first sampling after N.W. Latouche Is. Heavy oil/moderate HP/BR fertilizer addition; the populations on fertilized and unfertilized energy beaches were not significantly different at the other sampling times, N.
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