Microbial activities and dissolved organic matter dynamics in oil-contaminated surface seawater from the Deepwater Horizon oil spill site

Abstract

The Deepwater Horizon oil spill triggered a complex cascade of microbial responses that reshaped the dynamics of heterotrophic carbon degradation and the turnover of dissolved organic carbon (DOC) in oil contaminated waters. Our results from 21-day laboratory incubations in rotating glass bottles (roller bottles) demonstrate that microbial dynamics and carbon flux in oil-contaminated surface water sampled near the spill site two weeks after the onset of the blowout were greatly affected by activities of microbes associated with macroscopic oil aggregates. Roller bottles with oil-amended water showed rapid formation of oil aggregates that were similar in size and appearance compared to oil aggregates observed in surface waters near the spill site. Oil aggregates that formed in roller bottles were densely colonized by heterotrophic bacteria, exhibiting high rates of enzymatic activity (lipase hydrolysis) indicative of oil degradation. Ambient waters surrounding aggregates also showed enhanced microbial activities not directly associated with primary oil-degradation (β-glucosidase; peptidase), as well as a twofold increase in DOC. Concurrent changes in fluorescence properties of colored dissolved organic matter (CDOM) suggest an increase in oil-derived, aromatic hydrocarbons in the DOC pool. Thus our data indicate that oil aggregates mediate, by two distinct mechanisms, the transfer of hydrocarbons to the deep sea: a microbially-derived flux of oil-derived DOC from sinking oil aggregates into the ambient water column, and rapid sedimentation of the oil aggregates themselves, serving as vehicles for oily particulate matter as well as oil aggregate-associated microbial communities.

Figure 1. Photo of an oil aggregate formed in one of the roller bottles.

Oil aggregate attached to surface water oil slick through sticky oil gels. Photo was taken at the end of the 21-day roller table incubation in one of the roller bottles containing seawater and oil (SW+oil1). Scale bar is approximately 10 mm.

Figure 2. Microbial cell numbers in roller bottle ambient waters.

Average microbial cell numbers in (A) uncontaminated and (B) oil-amended ambient water. Error bars represent standard deviations of 10 counting fields. Note that there are no cell counts available for control SW at day 2, SW1 at day 0 and day 10, SW+oil1 at day 2, and control SW+oil at day 0 and day 2.

Figure 3. Enzyme activities in roller bottle ambient waters.

Average potential hydrolysis rates (n = 3 ± standard deviation) in uncontaminated (A, C, E, G) and oil-amended (B, D, F, H) ambient waters. Note the different scales on the y-axis.

Figure 4. Aggregate-associated enzyme activities at the end of the incubation.

Average potential hydrolysis rates (n = 3 ± standard deviation) in oil aggregates after the 21-day roller table incubation. Letters indicate results from one-way ANOVA followed by the Bonferroni-Holmes test. Rates with the same letter are statistically indistinguishable. Note the different scales on the y-axis.

Figure 5. DOC and CDOM in roller bottle ambient water.

Dissolved organic carbon (DOC) concentration (A and B; n = 6 ± standard deviation) and colored dissolved organic matter (CDOM) fluorescence (maximum fluorescence peak; C, D) during the 21-day roller table incubation. Note that CDOM fluorescence was not measured in SW1 and SW+oil1. There are no data available on CDOM fluorescence for control SW at day 21.

Figure 6. Excitation-emission matrices (EEMs) for day 0 and day 21; note difference in scale among panels.

(A) SW+oil2, day 0; (B) SW+oil2, day 21; (C) control SW+oil, day 0; (D) control SW+oil, day 21; (E) SW2, day 0; (F) SW2, day 21; (G) control SW, day 0; (H) control SW, day 16 (there are no data available for day 21). The fluorescence intensities in oil-amended bottles (panels B and D) at day 21 were one order of magnitude higher than for all other samples.